phylogeny and classiﬁcation of...

Phylogeny and classification of Rosaceae

D. Potter1, T. Eriksson

2, R. C. Evans

3, S. Oh

4, J. E. E. Smedmark

2, D. R. Morgan

5, M. Kerr

6,

K. R. Robertson7, M. Arsenault

8, T. A. Dickinson

9, and C. S. Campbell

8

1Department of Plant Sciences, Mail Stop 2, University of California, Davis, California, USA2Bergius Foundation, Royal Swedish Academy of Sciences, Stockholm, Sweden3Biology Department, Acadia University, Wolfville, Nova Scotia, Canada4Department of Biology, Duke University, Durham, North Carolina, USA5Department of Biology, University of West Georgia, Carrollton, Georgia, USA6Department of Cell Biology and Molecular Genetics, University of Maryland, Maryland, USA7Center for Biodiversity, Illinois Natural History Survey, Champaign, Illinois, USA8Department of Biological Sciences, University of Maine, Orono, Maine, USA9Department of Natural History, Royal Ontario Museum, Toronto, Canada

Received January 17, 2006; accepted August 17, 2006Published online: June 28, 2007� Springer-Verlag 2007

Abstract. Phylogenetic relationships among 88genera of Rosaceae were investigated using nucle-otide sequence data from six nuclear (18S, gbssi1,gbssi2, ITS, pgip, and ppo) and four chloroplast(matK, ndhF, rbcL, and trnL-trnF) regions, sepa-rately and in various combinations, with parsimonyand likelihood-based Bayesian approaches. Theresults were used to examine evolution of non-molecular characters and to develop a new phylo-genetically based infrafamilial classification. As inprevious molecular phylogenetic analyses of thefamily, we found strong support for monophyly ofgroups corresponding closely to many previouslyrecognized tribes and subfamilies, but no previousclassification was entirely supported, and relation-ships among the strongly supported clades wereweakly resolved and/or conflicted between somedata sets. We recognize three subfamilies in Ros-aceae: Rosoideae, including Filipendula, Rubus,Rosa, and three tribes; Dryadoideae, comprisingthe four actinorhizal genera; and Spiraeoideae,comprising Lyonothamnus and seven tribes. Allgenera previously assigned to Amygdaloideae and

Maloideae are included in Spiraeoideae. Threesupertribes, one in Rosoideae and two in Spiraeoi-deae, are recognized.

Key words: Rosodae, Pyrodae, Kerriodae, chro-mosome number, fruit type.

Introduction

In spite of general familiarity with and interestin the family, phylogenetic relationshipsamong taxa within Rosaceae have remainedpoorly understood and to date no infrafamilialclassification has been proposed thatrecognizes only groups strongly supported asmonophyletic. Moreover, although theapproximately 90 genera and 3,000 speciesthat are now generally accepted as belongingto the family have long been included in it,circumscription of Rosaceae, in terms of theinclusion or exclusion of other taxa, has varied

Pl. Syst. Evol. 266: 5–43 (2007)DOI 10.1007/s00606-007-0539-9Printed in The Netherlands

Plant Systematicsand Evolution

among the major treatments of the familyproposed over the last 60 years (Potter 2003).Taxa currently assigned to families Chrysoba-lanaceae (Malpighiales), Neuradaceae (Malva-les), and Quillajaceae (Fabales) (Morgan et al.1994, Angiosperm Phylogeny Group 2003)were all at one time included within Rosaceae(e.g. Lawrence 1951, Hutchinson 1964), thelast as recently as Takhtajan’s (1997) treatmentof the family. The single species of ApopetalumPax, listed in tribe Spiraeeae by Hutchinson(1964), was later determined (Cuatrecasas1970) to be a species of Brunellia (Brunellia-ceae, Oxalidales). Most recently, Oh andPotter (2006) showed that Guamatela Donn.Sm., previously classified in tribe Neillieae ofRosaceae (Hutchinson 1964), is most closelyrelated to species in the order Crossosoma-tales.

Molecular phylogenetic studies (Morgan etal. 1994, Evans et al. 2000, Potter et al. 2002)have provided strong support for monophylyof Rosaceae. Despite a long tradition ofgrouping these genera together, there is noreadily identifiable morphological synapomor-phy for the family. Presence of an hypanthiumand reduction or lack of endosperm are bothprobably synapomorphies for the order Ro-sales, and hence symplesiomorphies of Rosa-ceae (Judd and Olmstead 2004). Numerousstamens is a possible synapomorphy for thefamily (Judd and Olmstead 2004); if so, stamennumber has been secondarily reduced severaltimes within Rosaceae.

The position of Rosaceae with respect toother angiosperm families has varied amongtaxonomic treatments over the last century andhas been substantially affected by recent molec-ular phylogenetic studies. Besides Chrysoba-lanaceae and/or Neuradaceae, which, asmentioned above, were sometimes includedwithin Rosaceae, previous treatments haveincluded in Rosales Saxifragaceae, Crassula-ceae, andCunoniaceae (e.g., Cronquist 1981) orDichapetalaceae and Calycanthaceae (Hutch-inson 1964), none of which molecular evidencesupports as being particularly closely relatedto Rosaceae. The current circumscription of

Rosales (Angiosperm Phylogeny Group 2003)includes Barbeyaceae, Cannabaceae, Dirachm-aceae, Elaeagnaceae, Moraceae, Rhamnaceae,Rosaceae, Ulmaceae, and Urticaceae. Molecu-lar evidence indicates that Rosaceae are sisterto the remaining families in the order(Soltis et al. 2000, Potter 2003, Judd andOlmstead 2004).

Classification within Rosaceae also variesconsiderably among treatments (Table 1). Themost widely adopted classification (Schulze-Menz 1964) is primarily based on fruit typeand has four subfamilies, which are furtherdivided into tribes and subtribes. Hutchinson(1964), on the other hand, recognized onlytribes and did not group these into subfamilies.Takhtajan (1997), incorporating some of theresults of the first molecular phylogeneticstudy of relationships across Rosaceae (Mor-gan et al. 1994), recognized twelve subfamilies.In Takhtajan’s treatment, Amygdaloideae andMaloideae were expanded, and Rosoideae andSpiraeoideae were subdivided, as compared toearlier classifications. The treatment of Rosa-ceae by C. Kalkman, published posthumouslyby Kubitzki (2004, Kalkman 2004), recognizesonly tribes within Rosaceae. Kalkman, how-ever, suggested the possibility of recognizingtwo subfamilies, one comprising the classicalRosoideae and Prunoideae (hereafter, Amy-gdaloideae), the other the classical Maloideaeand Spiraeoideae. This would represent arather different treatment than the oneadopted here, in which the circumscription ofRosoideae is narrower than in most previoustreatments, Dryadoideae is recognized as aseparate subfamily, and Spiraeoideae is ex-panded to include the classical Amygdaloideaeand Maloideae. Kalkman’s treatment includesmore comprehensive surveys of vegetative andreproductive morphology, karyology, repro-ductive behavior, ecology, phytochemistry,economic uses, and conservation issues thanis possible here. In addition to the tribesadopted from earlier treatments, Kalkmandesignated three informal groups around thegenera Alchemilla, Geum, and Cydonia(Table 1). Adenostoma, Coleogyne, Potaninia,

6 D. Potter et al.: Phylogeny and classification of Rosaceae

Table

1.Comparisonofthenew

classificationforRosaceaepresentedherewithfourpreviouslypublished

classificationsofthefamily.Par-

entheses

aroundagroupofgenericnames

within

acolumnindicatesthat,in

thattreatm

ent,those

generawereincluded

inthegenuslisted

directly

abovethem

.A

notationof—

indicatesthatthegenuswasnotmentioned

inthetreatm

ent,or,in

thecase

ofthispaper,thatthegenushasnotbeen

representedin

anyphylogenetic

studyofthefamilyto

date.Superscripts

are

usedasfollows:

Letters

indicate

casesin

whichdifferencesin

placementofagenusin

differenttreatm

ents

precluded

thepossibilityofaligningthem

inthetable;RomanandArabic

numerals,respectively,

indicate

casesin

whichtribes

andsubfamilieshadto

besplitwithin

atreatm

ent.Taxonomic

authorities

forsupertribes,tribes,subtribes,and

generaare

included

inthetaxonomic

treatm

entsectionoftheDiscussion

ThisPaper

Schulze-Menz(1964)

Hutchinson(1964)

Takhtajan(1997)

Kalkman(2004)

Rosoideae

RosoideaeI

Fillpenduloideae

Ulm

arieae

Ulm

arieae

Ulm

arieae

Filipendula

Filipendula

Filipendula

Filipendula

Filipendula

Rosoideae

Rosodae

Roseae

Roseae

Roseae

Rosa

Rosa

Rosa

Rosa

Rosa

(Hulthem

ia)

(Hulthem

ia)

(Hulthem

ia)

Hulthem

ia(Hulthem

ia)

Rubeae

Rubeae

Ruboideae

Rubeae

Rubus

Rubus

Rubus

Rubus

Rubus

(Dalibarda)

Dalibarda

(Dalibarda)

(Dalibarda)

Potentilloideae

Sanguisorbeae

Sanguisorbeae

Poterieae

Sanguisorbeae

Sanguisorbeae

Agrimoniinae

Agrimoniinae

Agrimonia

Agrimonia

Agrimonia

Agrimonia

Agrimonia

Aremonia

—Aremonia

Aremonia

Aremonia

Hagenia

Hagenia

Hagenia

Hagenia

Hagenia

Leucosidea

—Leucosidea

Leucosidea

Leucosidea

Spenceria

—Spenceria

Spenceria

Spenceria

Sanguisorbinae

Sanguisorbinae

Acaena

Acaena

Acaena

Acaena

Acaena

Cliffortia

Cliffortia

Cliffortia

Cliffortia

Cliffortia

Margyricarpus

Margyricarpus

Margyricarpus

Margyricarpus

Margyricarpus

(Tetraglochin)

—Tetraglochin

Tetraglochin

(Tetraglochin)

Polylepis

Polylepis

Polylepis

Polylepis

Polylepis

Sanguisorba

Sanguisorba

Sanguisorba

Sanguisorba

Sanguisorba

Poteridium

—Poteridium

—(Poteridium,

Poterium

Poterium

Poterium

—Poterium)

(Bencomia,

—Bencomia

Bencomia

Bencomia

D. Potter et al.: Phylogeny and classification of Rosaceae 7

Table

1.(C

ontinued)

ThisPaper

Schulze-Menz(1964)

Hutchinson(1964)

Takhtajan(1997)

Kalkman(2004)

Marcetella,

——

—Marcetella,

Dendriopoterium,

——

—Dendriopoterium)

Sarcopoterium)

—Sarcopoterium

Sarcopoterium

Sarcopoterium

seebelowa

seebelowa

Alchem

illa

aseebelowa

seebelowa

Potentilleae

Potentilleae

Potentilleae

Potentilleae

Potentilleae

Potentillineae

Potentilla

Potentilla

Potentilla

Potentilla

Potentilla

(Argentina,

—Argentina

——

Comarella,

—Comarella

—(Comarella,

Duchesnea,

Duchesnea

Duchesnea

Duchesnea

Duchesnea,

Horkelia,

Horkelia

Horkelia

Horkelia

Horkelia,

Horkeliella,

—Horkeliella

Horkeliella

Horkeliella,

Ivesia,

Ivesia

Ivesia

Ivesia

Ivesia,

Purpusia,

—Purpusia

—Purpusia,

Stellariopsis)

—Stellariopsis

—Stellariopsis

Fragariinae

Alchem

illinae

Comarum

Comarum

Comarum

Comarum

Comarum,

(Farinopsis)

——

——

Dasiphora

—Pentaphylloides

——

Drymocallis

—Drymocallis

—Drymocallis,

Sibbaldia

—Sibbaldia

Sibbaldia

Sibbaldia,

Sibbaldiopsis

—Sibbaldiopsis

—Sibbaldiopsis)

Chamaerhodos

—Chamaerhodos

Chamaerhodos

Chamaerhodos

Fragaria

Fragaria

Fragaria

Fragaria

Fragaria

Alchem

illeae

Alchem

illa

Group

Alchem

illa

Alchem

illa

seeabovea

Alchem

illa

Alchem

illa

(Aphanes,

Aphanes

—Aphanes

(Aphanes,

Lachem

illa,

Lachem

illa

——

Lachem

illa,

Zygalchem

illa)

——

—Zygalchem

illa)

uncleartribalposition

Potaninia

b—

seebelowb

seebelowb

Potaninia

b

Sibbaldianthe

——

——

(Schistophyllidium)

——

——

Colurieae

Dryadeae

Dryadeae

Geeae

Geum

Group

Geinae

Geum

Geum

Geum

Geum

Geum


(Acomastylis,

(Acomastylis,

Acomastylis

—Acomastylis

Novosieversia,

—Novosieversia

Novosieversia

(?N

ovosieversia)

Oncostylus,

Oncostylus)

——

Oncostylus

Orthurus,

—Orthurus

Orthurus

Orthurus

——

——

Parageum

Taihangia,

——

Taihangia

(?T

aihangia)

Coluria,

Coluria

Coluria

Coluria

Coluria

Doubtfullyin

Geum

Group

Waldstenia)

Waldsteinia

Waldsteinia

Waldsteinia

Waldsteinia

Sieversia

—Sieversia

Sieversia

Sieversia

Dryadinae

Dryadeae

Fallugia

Fallugia

Fallugia

Fallugia

Fallugia

Dryadoideae

Dryadeae

Dryas

Dryas

Dryas

Dryas

Dryas

Purshiinae

Purshieae

Chamaebatia

Chamaebatia

Chamaebatia

Chamaebatia

Chamaebatia

Purshia

Purshia

Purshia

Purshia

Purshia

(Cowania)

Cowania

Cowania

Cowania

Cowania

Cercocarpinae

Cercocarpeae

Cercocarpeae

Cercocarpus

Cercocarpus

Cercocarpus

Cercocarpus

Cercocarpus

Potaninieae

seeaboveb

—Potaninia

bPotaninia

bseeaboveb

seebelowc

seebelowc

Coleogynec

seebelowc

seebelowc

Spiraeoideae

Lyonothamnoideae

Quillajeae2


Lyonothamnusd

seebelowd

Lyonothamnusd

Lyonothamnusd

Lyonothhamnusd

Kerriodae

Coleogynoideae

Kerrieae

Kerrieae


Coleogyne

Coleogyne

seeabovec

Coleogyne

Coleogyne

Kerrioideae

Kerrieae

Kerrieae

Kerrieae

Kerria

Kerria

Kerria

Kerria

Kerria

Neviusia

Neviusia

Neviusia

Neviusia

Neviusia

Rhodotypeae

Rhodotypeae

Rhodotypos

Rhodotypos

Rhodotypos

Rhodotypos

Rhodotypos


Table

1.(C

ontinued)

ThisPaper

Schulze-Menz(1964)

Hutchinson(1964)

Takhtajan(1997)

Kalkman(2004)

SpiraeoideaeII

Amygdaloideae

Osm

aronieae

Exochordeae1

Quillajeae2

Exochordeae

Exochordeae3

Exochorda

Exochorda

Exochorda

Exochorda

Exochorda

Prunoideae

Osm

aronieae

Osm

aronieae

Pruneae

Oem

leria

Oem

leria

Oem

leria(asOsm

aronia)

Oem

leria

Oem

leria

Pruneae

Prinsepieae

Prinsepia

Prinsepia

Prinsepia

Prinsepia

Prinsepia

(Plagiospermum)

—Plagiospermum

—(Plagiospermum)

Amygdaleae

Amygdaleae

Prunus

Prunus

Prunus

Prunus

Prunus

(Arm

eniaca,

(Arm

eniaca,

(Arm

eniaca,

Arm

eniaca

—Cerasus,

Cerasus,

Cerasus)

Cerasus

(Cerasus,

Amygdalus,

Amygdalus,

Amygdalus

Amygdalus

Amygdalus,

Padus,

Padus,

Padus

Padus

Padus,

Laurocerasus,

Laurocerasus)

Laurocerasus

Laurocerasus

Laurocerasus,

Pygeum,

Pygeum

Pygeum

Pygeum

Pygeum)

Maddenia)

Maddenia

Maddenia

Maddenia

Maddenia

RosoideaeI

Spiraeoideae

Sorbarieae

Adenostomeae

Adenostomateae

Adenostomateae


Adenostoma

Adenostoma

Adenostoma

Adenostoma

Adenostoma

SpiraeoideaeII

Sorbarieae

Gillenieae4

Sorbarieae

Gillenieae4

Sorbaria

Sorbaria

Sorbaria

Sorbaria

Sorbaria

Chamaebatiaria

Chamaebatiaria

Chamaebatiaria

Chamaebatiaria

Chamaebatiaria

seeaboved

Lyonothamnusd

See

aboved

seeaboved

seeaboved

Spiraeanthuse

seebelowe

Spiraeanthuse

seebelowe

Spiraeanthuse

Spiraeeae

Spiraeeae

Spiraeeae

Spiraeeae

Spiraeeae

Aruncus

Aruncus

Aruncus

Aruncus

Aruncus

Kelseya

—Kelseya

Kelseya

Kelseya

Luetkea

—Luetkea

Luetkea

Luetkea

(asEriogynia)

Petrophyton

—Petrophyton

Petrophyton

Petrophyton

(asPetrophytum)

Sibiraea

Sibiraea

Sibiraea

Sibiraea

Sibiraea

Spiraea

Spiraea

Spiraea

Spiraea

Spiraea


——

(Pentactina)

Pentactina

(Pentactina)

Xerospiraea

——

—Xerospiraea

Holodisceae

Holodisceae

Holodisceae

Holodiscus

Holodiscus

Holodiscus

Holodiscus

Holodiscus

Neillieae

Neillieae

Neilieae

Neillieae

Neillieae

Physocarpus

Physocarpus

Physocarpus

Physocarpus

Physocarpus

Neillia

Neillia

Neillia

Neillia

Neillia

(Stephanandra)

Stephanandra

Stephanandra

Stephanandra

Stephanandra

Pyrodae

Gillenieae

Gillenieae4

Gillenieae

Gillenieae4

Gillenia

Moench.

Gillenia

Gillenia

(asPorteranthus)

Gillenia

Gillenia

seeabovee

Spiraeanthuse

See

abovee

Spiraeanthuse

seeabovee

Pyroideae

Pyreae

Quillajeae2

Quillajeae2

Kageneckieae

Exochordeae3

Kageneckia

Kageneckia

Kageneckia

Kageneckia

Kageneckia

Lindleyieae

Vauquelinia

Vauquelinia

Vauquelinia

Vauquelinia

Vauquelinia

Exochordeae1

Lindleya

Lindleya

Lindleya

Lindleya

Lindleya

Pyrinae

Maloideae

Maleae

Pomeae

Maleae

Maleae5

Amelanchier

Amelanchier

Amelanchier

Amelanchier

Amelanchier

Malacomeles

—Malacomeles

Malacomeles

(Malacomeles,

Peraphyllum

—Peraphyllum

Peraphyllum

Peraphyllum)

Aronia

—Aronia

Aronia

Aronia

Photinia

Photinia

Photinia

Photinia

(Photinia)

Docyniopsis

——

Docyniopsis

Macromeles

Eriobotrya

Eriobotrya

Eriobotrya

Eriobotrya

Eriobotrya

Eriolobus

—Eriolobus

Eriolobus

Eriolobus

Heteromeles

——

Heteromeles

Heteromeles

Malus

Malus

Malus

Malus

Malus

Stranvaesia

Stranvaesia

Stranvaesia

(Stranvaesia)

(Stranvaesia)

Pyrus

Pyrus

Pyrus

Pyrus

Pyrus

Rhaphiolepis

Rhaphiolepis

Rhaphiolepis

Rhaphiolepis

Rhaphiolepis

Sorbus

Sorbus

Sorbus

Sorbus

Sorbus

Aria

——

—(A

ria,

Chamaem

espilus

——

Chamaem

espilus

Chamaem

espilus,

Corm

us

——

Corm

us

Corm

us,

Torm

inalis

——

Torm

inalis

Torm

inalis)


and Lyonothamnus were not assigned to tribes.Both Guamatela and Brachycaulos Dikshit &Panagrahi are listed as ‘‘doubtfully Rosacea-ous.’’ The latter genus is known only from asingle collection from India (Kalkman 2004)and will not be considered further in thispaper.

Studies of phylogenetic relationships with-in Rosaceae based upon molecular data haveagreed in providing strong support for severalclades that more or less correspond to previ-ously recognized subfamilies and tribes and inshowing rather weak support for the relation-ships among those clades. Morgan et al.’s(1994) phylogenetic analysis of rbcL sequencevariation across the family resolved as mono-phyletic groups that corresponded, with a fairnumber of modifications, to Schulze-Menz’s(1964) Rosoideae, Amygdaloideae, andMaloideae, but Spiraeoideae were polyphy-letic. The results suggested that, in Rosaceae,chromosome number is a better indicator ofrelationship than is fruit type. Taxa with x= 9traditionally assigned to Rosoideae becausetheir members produce achenes were found tofall outside of Rosoideae sensu stricto (x = 7,8), whereas several taxa with x = 15 and 17traditionally classified in Spiraeoideae becausethey produce follicles were found to be moreclosely related to pome-bearing Maloideae.Prunus (x = 8, drupes) was weakly supportedas sister to a strongly supported clade of threeother genera with the same base chromosomenumber; members of two of those genera(Oemleria and Prinsepia) also bear drupes,but those of the third, Exochorda, producecapsules (more accurately, cocceta; seeResults).

Analyses of chloroplast ndhF sequences(Evans 1999) and morphological and ontoge-netic characters (Evans 1999; Evans andDickinson 1999a, 1999b) provided supportfor many of the clades that were also stronglysupported by Morgan et al.’s (1994) study.Potter et al.’s (2002) analyses of chloroplastmatK and trnL-trnF sequences also resolvedmost of these clades but differed in details ofthe relationships among them, though most ofT

able

1.(C

ontinued)

ThisPaper

Schulze-Menz(1964)

Hutchinson(1964)

Takhtajan(1997)

Kalkman(2004)

Cydonia

Group

Chaenomeles

Chaenomeles

Chaenomeles

Chaenomeles

Chaenomeles

Cydonia

Cydonia

Cydonia

Cydonia

Cydonia

Docynia

—Docynia

Docynia

Docynia

Pseudocydonia

—Pseudocydonia

Pseudocydonia

Pseudocydonia

Crataegeae

Crataegeae

Crataegeae

Chamaem

eles

—Chamaem

eles

Chamaem

eles

Chamaem

eles

Cotoneaster

Cotoneaster

Cotoneaster

Cotoneaster

Cotoneaster

Crataegus

Crataegus

Crataegus

Crataegus

Crataegus

Hesperomeles

—Hesperomeles

Hesperomeles

Hesperomeles

Mespilus

Mespilus

Mespilus

Mespilus

Mespilus

Osteomeles

—Osteomeles

Osteomeles

Osteomeles

Pyracantha

Pyracantha

Pyracantha

Pyracantha

Pyracantha

Dichotomanthoideae

Maleae5

Dichotomanthes

—Dichotomanthes

Dichotomanthes

Dichotomanthes


those relationships were not well supported byany of the analyses. One important differenceconcerned relationships among basally diverg-ing lineages in the family. The rbcL dataprovided weak support for a sister relationshipbetween Rosoideae sensu stricto and the rest ofthe family, while in the strict consensus treebased on matK and trnL-trnF data, threeclades formed an unresolved polytomy diverg-ing at the base of the family: Rosoideae sensustricto, the actinorhizal taxa (Dryadoideae incolumn 1 of Table 1), and the rest of the family(Spiraeoideae in column 1 of Table 1). Withinthe last clade, there was strong support for asister relationship between Lyonothamnus andthe remaining taxa.

Studies of granule-bound starch synthasegene (gbssi) sequences by Evans et al. (2000)and Evans and Campbell (2002) were aimedprimarily at investigating the origins ofMaloideae. This group has long attracted theattention of evolutionary biologists because ofthe possibility that it may represent a higher-level angiosperm group of hybrid origin, assuggested by chromosome numbers and iso-zyme data (Chevreau et al. 1985, Chevreau andLaurens 1987, Weeden and Lamb 1987, Raspeet al. 1998). A particularly intriguing hypoth-esis holds that the base chromosome numberof x =17 in this group resulted from widehybridization between an ancestral amygda-loid with x= 8 and an ancestral spiraeoid withx = 9 (Sax 1933). Data from the low copynuclear gene gbssi provide an excellent tool totest this hypothesis. This gene has undergone aduplication prior to the evolution of Rosaceae(Evans et al. 2000), with two copies found inall diploid taxa with x = 7, 8, or 9, andanother duplication (as a result of ancientpolyploidization) within Rosaceae, resulting infour copies in diploid taxa with x = 15 or 17.Phylogenetic analyses of these genes for abroad sampling of taxa with the differentchromosome numbers from across the family(Evans and Campbell 2002) did not supportthe wide-hybridization hypothesis. Instead,both gbssi1 and gbssi2 resolved Gillenia(x = 9) as sister to the clade including taxa

with x = 15 or 17, a result also supported bythe ndhF (Evans 1999) and matK/trnL-trnF(Potter et al. 2002) data; Gillenia was notsampled by Morgan et al. (1994). These resultsare consistent with a spiraeoid origin ofMaloideae (Sterling 1966, Gladkova 1972),and they support an alternative to the wide-hybridization hypothesis, which holds that thehigher chromosome number of maloids arosevia hybridization and polyploidization amongclosely related species of an ancestral lineage(the lineage that also gave rise to Gillenia withx = 9), followed by aneuploid reduction. Theresults further suggest a New World origin ofthis group, since Gillenia, Lindleya, and Vau-quelinia are all distributed in North America,and Kageneckia is found in South America.Finally, these results support recognition of ataxon (here designated supertribe Pyrodae;Table 1) including not only all genera withchromosome numbers of 15 and 17 (Takhta-jan’s (1997) Pyroideae, our Pyreae; Table 1)but also Gillenia with x = 9. Outside of thisexpanded maloid group, the gbssi results(Evans and Campbell 2002) resolved severalof the same groups of genera that wereidentified in other molecular phylogeneticstudies of the family (Morgan et al. 1994,Evans 1999, Potter et al. 2002) but, once again,provided generally weak resolution of rela-tionships among those groups.

The objectives of the present study are to1) assemble molecular phylogenetic data forRosaceae which have been generated inseveral labs in North America and Europeover the last 10–15 years; 2) analyze thesedata separately and in combination in orderto determine the extent to which differentdata sets may conflict with one another andto obtain the best hypotheses of phylogeneticrelationships in the family according tocurrently available evidence; 3) explore theimplications of the phylogenetic trees gener-ated from molecular data for the evolution ofstructural, biochemical, and ecological char-acters; and 4) produce a new, phylogeneti-cally based infrafamilial classification forRosaceae.


Materials and methods

Data. Ten genes or genomic regions were analyzedin this study (Table 2), including six nuclear andfour chloroplast loci. The six nuclear loci are: 18Sribosomal RNA genes, internal transcribed spacer(ITS) regions (including ITS 1, the 5.8S ribosomalRNA gene, and ITS 2), gbssi1 and gbssi2, andputative genes encoding polygalacturonase inhibi-tor proteins (PGIP) and polyphenol oxidase (PPO).The four chloroplast loci are: rbcL, matK, ndhF,and trnL-trnF.

The taxa sampled for each locus are listed inTable 2. Many of the sequences used in this studywere included in previously published analyses;for those that were not, voucher specimeninformation is given in Table 2, or, for generaof Pyreae, in Campbell et al. (2007). Methods forDNA extraction, PCR amplification, cloning(where necessary) and sequencing of particularloci may be found in the publications listed inTable 2. Data from several loci are published herefor the first time, and the methods for PCR andsequencing of these regions are described brieflybelow.

18S: GenBank 18S sequence of Prunus persica(L28749), Spiraea x vanhoutei (U42801), and Photi-nia fraseri (U42800) were used to design a forward(18S1F: GACTGTGAAACTGCGAATGGCTC)and a reverse PCR primer (18S2R: GTTCACCTACGGAAACCTTGTTACG) as well as twointernal primers (18S3F: TAACGAGGATCCATTGGAGG and 18S4R: AGATCCACCAACTAAGAACG), which were purchased from SigmaGenosys, Inc. and Integrated DNA Technologies,Inc. Approximately 1.6 kb of the 18S gene wereamplified from extracted genomic DNA of eachtaxon in 25 ll reactions containing 2.5 lL of 100Xbovine serum albumin (BSA), 2.5 lL of 10Xpolymerase buffer, 3 lL of 25 mM MgCl2, 0.5 lLof 10 mM dNTPs, 0.75 lL of each 10 mM primer,1.0 unit of Taq DNA polymerase (mostly fromPromega Inc.), and 15–60 ng of genomic DNA.PCR conditions were as follows: 30 cycles of 94�Cfor 1.5 min, 55�C for 2 min, and 72�C for 2 min,followed by 72�C for 15 min. PCR products werepurified from agarose gels with the Qiaquick GelExtraction Kit (Qiagen Inc.). PCR products weresequenced directly in both directions using bothexternal and internal primers on an ABI/Prism 377automated sequencer at the University of MaineDNA Sequencing Facility.

pgip: Sequences of PGIPs from several eudicots(Malus domestica, Yao et al. 1995; Phaseolusvulgaris L., Toubart et al. 1992; Actinidia deliciosa(A. Chev.) Liang and A. R. Ferg., Simpson et al.1995; Pyrus communis, Stotz et al. 1993; andLycopersicon esculentum Miller, Stotz et al. 1994)were obtained from GenBank, aligned, and used todesign two forward (PGIP1: TCCTCCTACAAAT-CAAGAAAG and PGIP5: CCAGCTCTCTCT-GATCTCTGCAACCC) and two reverse PCRprimers (PGIP2: TTGCAGCTTGGGAGTGGAGand PGIP6: ACCACACAGCCTGTTGTAGCT-CAC) as well as two internal sequencing primers(PGIP3: GACCGTAATAAGCTCACAGG andPGIP4: CCTGTGAGCTTATTACGGTC), whichwere purchased from Genosys Biotechnologies,Inc. Approximately 0.9 kb of the PGIP gene wasamplified from extracted genomic DNA of eachtaxon using the Perkin-Elmer GeneAmp II kit andvarious combinations of the PCR primers (someprimer combinations did not yield any product forsome taxa). PCR conditions were as follows: 1 minat 95�C; 40 cycles of 30 s at 95�C, 1 min at 55�C,and 2 min at 72�C; 7 min at 72�C. PCR productswere purified from agarose gels with the QiaquickGel Extraction Kit (Qiagen Inc.). PCR productswere either sequenced directly in both directions(using both external and internal primers asneeded), or first cloned using the InvitrogenTopo-TA Cloning Kit. For cloned PCR products,one to ten colonies were selected from eachtransformation reaction for sequencing in bothdirections with universal primers M13 or T7 andM13 Reverse or T3 and internal primers asnecessary. Automated sequencing was carried outat one of the two DNA sequencing facilities on theU.C. Davis campus, each of which uses an ABI/Prism 377 automated sequencer.

ppo: Based on a consensus of published cDNAor genomic sequences for PPO genes from variousspecies of Rosaceae (Boss et al. 1995; Chevalier etal. 1999; Haruta et al. 1998, 1999), three forward(PPO1: TAGACAGGAGAAATGTGCTTCTTGG, PPO3: GACCCGTTCGCCTTTGCCAAGCC, and PPO5: ATGACGTCTCTTTCACCT CCGGTAGTCAC) and two reverse (PPO2: CAC-TTACAAAGCTTCCGGCAAACTC and PPO6:TCCTCCGCCTCAATTTCCTCCAACA) PCRprimers were designed to amplify a fragment ofabout 1.5 kb, including most of the coding regionof the gene. Two internal sequencing primers


Table

2.Generegions(w

ithreferencesto

methodsforsequencing)andtaxasampledin

this

studywithpublicdatabase

accessionnumbers.

Voucher

inform

ationisprovided

incaseswhereithasnotpreviouslybeenpublished

Genus

18S(thisstudy;

voucher

in-

form

ationin

Evans1999or

Evansand

Campbell2002)

gbssi(Evanset

al.2000,Evans

andCampbell

2002,Smed-

mark

etal.

2003,2005;

Campbellet

al.

2006)

ITS(Bortiriet

al.2001,

Campbellet

al.

1995,Eriksson

etal.1998,

2003;Helfgott

etal.2000;

Smedmark

and

Eriksson2002;

Kerr2004;

Campbellet

al.

2006;this

study)

pgip(thisstudy)

ppo(thisstudy)

matK

(Potter

etal.

2002,Campbellet

al.2006)

ndhF

(Evans1999;

Campbellet

al.

2006;thisstudy;

additionalvoucher

inform

ationin

Evans1999and

EvansandCamp-

bell2002)

rbcL

(Morganet

al.

1994;thisstudy)

trnL-trnF(Potter

etal.2002;Erikssonet

al.2003;Smedmark

andEriksson2002;

Kerr2004;Camp-

bellet

al.2006;this

study)

Acaena

––

cylindristachya

Ruiz

&Pav.

AJ512775

––

––

–cylindri.

AJ512780

Adenostoma

fasciculatum

Hook.&

SArn.

DQ88363

fascic.

AF500389

fascic.O

h970424-01

(DAV)

DQ88358

fascic.Oh970424-

01(D

AV)

AF196866

fascic.Oh970424-

01(D

AV)

DQ851197

fascic.AF288095

fascic.

DQ851497

sparsifolium

Torr.

U06790

fascic.

AF348535

Agrimonia

––

eupatoriaL.

U90798

––

––

parviflora

Ait.

U06791

eupatoriaAJ512216

Alchem

illa

––

alpinaL.

U90816,

U90817

––

––

mollis(Buser)

Rothm.U06792

alpinaAJ512217

Amelanchier

–bartramiana

(Tausch)Roe-

mer

AF285973

–AF285976

DQ874881

DQ874907

DQ874909

bartram.

U151591

––

bartram.D

Q860450

bartram.D

Q851498

alnifoliaNutt.

U06793

bartram.

DQ863222

Aremonia

––

agrimonioides

(L.)DC.

U90799

––

––

–agrimon.

AJ512230,

AJ512231

Aria

–alnifolia(Sie-

bold

&Zucc.)

Decne.

AF500390-

AF500393

alnifoliaU16185

––

alnifoliaDQ860451

alnifoliaDQ851499

–alnifoliaDQ863223

Aronia

–arbutifolia(L.)

Elliott

AF500394–

AF500395

arbutifolia

U16199

––

arbutifolia

DQ860452

arbutifolia

DQ851500

–arbutifolia

DQ863224

Aruncus

–dioicus(Walter)

Fernald

AF285999–

AF286001

–dioicusU

CBot.

Gard.83.0466

AF196868

–dioicusAF288094

dioicusUC

Bot.

Gard.83.0466

DQ851501

sylvesterKostel.

U06794

dioicusAF348536

Ceanothus

sanguineus

Pursh.U42799

–gloriosusJ.

T.

Howell

AF398524

––

–americanusL.

DQ851502

sanguineusU06795

–


Table

2.(C

ontinued)

Cercocarpus

betuloides

Nutt.

DQ88364

betuloides

AF500396–

AF500397

betuloides

Gao

s.n.(D

AV)

DQ88355

betuloides

Gao

s.n.(D

AV)

AF196870

betuloides

Gao

s.n.(D

AV)

DQ851198

betuloides

AF288095

betuloides

Gao

s.n.(D

AV)

DQ851503

ledifoliusNutt.

exTorr.&

A.

GrayU06796

betuloides

AF348537

Chaenomeles

–speciosa

(Sweet)

Nakai

AF285977–

AF285979

AF500398

DQ874902

cathayensis

(Hem

sl.)C.K.

Schneid.

U16186

speciosa

UCD

Arboretum

A80.0005

AF196871

speciosa

UCD

Arboretum

A80.0005

DQ851199

cathayensis

DQ860453

speciosa

DQ851504

–cathayensis

DQ863225

Chamaebatia

foliolosa

Benth.

DQ88365

australis(Bdg.)

Abrams

DQ904401

foliolosa

Potter

970427-02

(DAV)

DQ88356

foliolosa

Potter

970427-02

(DAV)

AF196872

foliolosa

Potter

970427-02

(DAV)

DQ851200

foliolosa

AF288096

foliolosa

DXP

313Larsons.n.

(DAV)

DQ851505

–foliolosa

AF348538

Chamaebatiaria

millefolium

(Torr.)Maxim

.DQ88366

millefolium

AF500399–

AF500400

millefolium

UCD

Arb.

A74.0245

DQ88359

millefolium

UCD

Arb.

A74.0245

AF196874

millefolium

UCD

Arb.

A74.0245

DQ851201

millefolium

AF288097

millefolium

DQ851506

millefolium

U06797

millefolium

AF348539

Chamaem

eles

––

coriaceaLind-

leyDQ811768

––

coriacea

DQ860454

coriacea

DQ851507

–coriacea

DQ863226

Chamaem

espi-

lus

–alpina(M

iller)

Robertson&

Phipps

AF500401–

AF500404

alpina

DQ811769

––

alpina

DQ860455

alpina

DQ851508

–alpina

DQ863227

Chamaerhodos

––

erecta

(L.)

BungeU90794

––

––

–erecta

AJ512219

Cliffortia

––

odorata

L.f.

AY634874

––

––

–odorata

AY634724

Coleogyne

––

––

–ramosissim

aTorr.Potter

020913-01

(DAV)

DQ851224

––

–

Comarum

––

palustre

L.

AJ511777

––

––

–palustre

AJ512237

Corm

us

–domestica

Spach

AF500405-

AF500408

domestica

U16187

––

domestica

DQ860456

domestica

DQ851509

–domestica

DQ863228

Cotoneaster

–lacteusW.W.

Smith

AF500409-

AF500412

lacteusU16188

––

lacteus

DQ860457

apiculatus

Rehd.&

Wilson

DQ851510

–lacteus

DQ863229

Cowania

––

––

––

–stansburiana

Torr.U59817

–

Crataegus

–rivularisNutt.

AF500413-

AF500414

DQ874883

mollisScheele

U16190

monogynaJacq.

Potter

970517-

08(D

AV)

AF196879

monogynaPot-

ter970517-08

(DAV)

DQ851202

submollisSarg.

DQ860458

rivularis

DQ851511

columbianaHo-

wellU06799

submollis

DQ863230

Cydonia

–oblongaMiller

AF500415-

AF500416

DQ874910

oblongaU16189

––

oblonga

DQ860459

oblonga

DQ851512

–oblonga

DQ863231


Dasiphora

––

fruticosa

(L.)Rydb.

U90808,

U90809

fruticosa

culti-

varJ.

Lubys.n.

AF196918

fruticosa

culti-

varJ.

Lubys.n.

DQ851214

–fruticosa

DQ851513

fruticosa

U06818

fruticosa

AJ512233

Dichotomanthes

–tristaniicarpa

Kurz

AF500417-

AF500420

tristaniicarpa

DQ811770

––

tristaniicarpa

DQ860460

tristaniicarpa

DQ851514

–tristaniicarpa

DQ863232

Docyniopsis

–tschonskii

(Maxim

.)Koidzumi

AF500421-

AF500422

DQ874884

tschonskii

DQ811771

––

tschonskii

DQ860461

tschonskii

DQ851515

–tschonoskii

DQ863233

Dryas

–octopetala

L.

Smedmark

11

(S)AM116868

octopetala

U90804

––

octopetala

Pot-

ter011020-01

(DAV)

DQ851225

octopetala

Pot-

ter011020-01

(DAV)

DQ851516

drummondiiRi-

chards.ex

Hook.U59818

octopetala

Pot-

ter011020-01

(DAV)

DQ851231

Drymocallis

––

agrimonioides

(Pursh)Rydb.

U90787

––

––

–agrimonioides

AJ512223

Eriobotrya

–japonicaLindl.

AF500423-

AF500424

DQ874901

japonica

U16192

––

japonica

DQ860462

japonica

DQ851517

japonica

U06800

japonica

DQ863234

Eriolobus

–trilobata

Roe-

mer

AF500425

-AF500428

––

–trilobata

DQ860463

trilobata

DQ851518

–trilobata

DQ863235

Exochorda

racemosa

(Lindl.)Rehder

DQ88367

racemosa

AF286002-

AF286003

racemosa

AF318740

racemosa

UCD

Arb.AF196885

racemosa

UCD

Arb.DQ851203

racemosa

AF288100

racemosa

DQ851519

giraldiiHesse

U06801

racemosa

AF348542

Fallugia

–paradoxaEndl.

AJ871485T.

Eriksson796

(SBT)

AM116868

paradoxa

U90805

–paradoxaPotter

970428-01

(DAV)

DQ851204

paradoxa

AF288101

paradoxaPotter

970428-01

(DAV)

DQ851520

paradoxa

U06802

paradoxa

AJ297331

Filipendula

vulgaris

Moench

DQ88368

vulgaris

AJ871487T.

Eriksson821

(SBT)

AM116870

vulgaris

AJ416467

––

––

vulgarisU06804

vulgaris

AJ416463

Fragaria

ananassaRo-

zier

X15590

vescaL.

AJ871486

vescaAJ511771

vescaPotter

970209-01

(DAV)

AF196891

–vesca

AF288102

vesca

DQ851521

ananassa

U06805

vescaAJ512232

Geum

–urbanum

L.

AJ534193

Smedmark

3(S)

AM116871

urbanum

AJ302337

––

–macrophyllum

Willd.

DQ851522

chiloense

Balb.

L01921

urbanum

AJ297323

Gillenia

trifoliata

(L.)

Moench

DQ88369

trifoliata

(L.)

Moench

AF500431-

AF500432

DQ874890-

DQ874891

stipulata

(Muhl.

exWilld.)Baill.

DQ811763

stipulata

UC

Bot.Gard.

92.0438

AF196913

stipulata

UC

Bot.Gard.

92.0438

DQ851205

stipulata

AF288103

trifoliata

DQ851523

stipulata

DQ250747Ro-

bertsons.n.

(ILLS)

stipulata

AF348554


Table

2.(C

ontinued)

Hagenia

––

abyssinica

(Bruce)J.

F.

Gmel.U90800

––

––

–abyssinica

AY634727

Heteromeles

–arbutifoliaRoe-

mer

AF500433

-AF500435

arbutifolia

U16193

arbutifoliaGao

s.n.(D

AV)

AF196894

arbutifoliaGao

s.n.(D

AV)

DQ851207

arbutifolia

DQ860464

arbutifolia

DQ851524

–arbutifolia

DQ863236

Holodiscus

discolor(Pursh)

Maxim

.DQ88370

–microphyllus

Rydb.UCD

Arbor.

A89.0417

DQ88361

microphyllus

UCD

Arbor.

A89.0417

AF196895

microphyllus

UCD

Arbor.

A89.0417

DQ851208

discolor

AF288105

discolorPotter

970517-07

(DAV)

DQ851525

discolorU06807

discolor

AF348546

Kageneckia

–oblongaRuiz

&Pav.AF285980

-AF285982

DQ874892-

DQ874894

angustifoliaD.

DonDQ811764

oblongaUC

Bot.Gard.

88.0176

AF196898

oblongaUC

Bot.Gard.

88.0176

DQ851209

angustifolia

DQ860447

angustifolia

DQ851526

angustifolia

U06808

oblonga

AF348547

Kelseya

––

––

–uniflora

(S.

Wats.)Rydb.

D.Barton2218

(DAV)

DQ851226

––

uniflora

D.

Barton2218

DQ851232

Kerria

japonica(L.)

DC.AF132890

japonica

DQ904404

japonicaPotter

s.n.(D

AV)

DQ88360

––

–japonica

DQ851527

japonica

DQ250749

MortonArb.

Acc.466-78

–

Leucosidea

––

sericeaEckl.&

Zeyh.

AF183547,

AF183524

––

––

–sericea

AJ512222

Lindleya

–mespiloides

Kunth

AF500436-

AF500438

DQ874895

mespiloides

DQ811764

––

mespiloides

DQ860448

mespiloides

DQ851528

mespiloides

U06810

mespiloides

DQ863220

Luetkea

––

pectinata

(Pursh)Kunze

Morgan2284

(WWB)

DQ851235

––

pectinata

Potter

011020-02

(DAV)

DQ851227

–pectinata

Mor-

gan2284

(WWB)

DQ250750

pectinata

Mor-

gan2284

(WWB)

DQ851233

Lyonothamnus

floribundus

GrayDQ88371

floribundus

AF500439

floribundus

AY555315

floribundusGao

s.n.(D

AV)

AF196903

floribundusGao

s.n.(D

AV)

DQ851210

floribundus

AF288107

floribundus

Gaos.n.(D

AV)

DQ851529

floribundus

U06811

floribundus

AF348548

Maddenia

––

hypoleuca

Koehne

AF179549,

AF179550

––

hypoleuca

Lee

&Wen

5005

(CS)DQ851228

––

hypoleuca

AY864827

Malacomeles

–denticulata

(Kunth)Engler

AF500440-

AF500441

denticulata

U16194

––

denticulata

DQ860465

denticulata

DQ851520

–denticulata

DQ863237

Malus

–sargentiiRe-

hder

AF285983

-AF285985

AF500442

domestica

Borkh.U16195

––

sargentii

DQ860466

domestica

DQ851531

–sargentii

DQ863238


Margyricarpus

––

cristatusBrit-

ton.AJ512777

––

–pinnatus(Lam.)

Kuntze

DQ851532

–cristatus

AJ512782

Mespilus

–germanicaL.

AF500443-

AF500446

germanica

U16196

––

germanica

DQ860467

germanica

DQ851533

–germanica

DQ863239

Neillia

(Stephanandra

incisa

(Thunb.)

Zabel)

DQ88381

(Stephanandra

incisa)

AF500469

thyrsiflora

D.

DonAF487148

–thyrsiflora

DXP

170DQ851211

thyrsiflora

AF288108

sinensisOliv.

DXP103

DQ851534

sinensisU06813

thyrsiflora

AF487229

Neviusia

alabamensisA.

GrayDQ88372

––

alabamensisUC

Bot.Gard.

93.0973

AF196906

–alabamensis

AF288109

alabamensis

DQ851535

alabamensis

U06815

alabamensis

AF348550

Oem

leria

–cerasiform

is(Torr.&

Gray

exHook.&

Arn.)Landon

AF285986

cerasiform

isAF318715

–cerasiform

isBortiri129

(DAV)

DQ851212

cerasiform

isAF288110

cerasiform

isBortiri129

(DAV)

DQ851536

cerasiform

isU06816

cerasiform

isAF348551

Osteomeles

–anthyllidifolia

L.AF285987-

AF285988

DQ874888-

DQ874889

schwerinae

Schneider

U16197

––

schwerinae

DQ860468

schwerinae

DQ851537

–schwerinae

DQ863240

Peraphyllum

–ramosissim

um

Nutt.

AF500447-

AF500449

DQ874903

ramosissim

um

U16198

––

ramosissim

um

DQ860469

ramosissim

um

DQ851538

–ramosissim

um

DQ863241

Petrophyton

––

caespitosum

(Nutt.)Rydb.

Potter

020906-

02(D

AV)

DQ851236

––

caespitosum

Potter

020906-

02(D

AV)

DQ851229

––

caespitosum

Potter

020906-

02(D

AV)

DQ851234

Photinia

fraseri

Dress

U42800

villosa

(Thunb,)

DC.AF500450

-AF500452

–serrulata

Lindl.

UC

DavisPot-

ter970911-01

AF196907

–villosa

DQ860470

villosa

DQ851539

fraseriL11200

villosa

DQ863242

Physocarpus

opulifolius(L.)

Maxim

.DQ88373

opulifolius

AF285989

opulifolius

AY555326

capitatus

(Pursh)Kuntze

Potter

970702-

01(D

AV)

AF196908

capitatusPotter

970702-01

(DAV)

DQ851213

capitatus

AF288112

opulifolius

DQ851540

malvaceus

(Greene)

KuntzeU06817

capitatus

AF348553

Polylepis

––

tarapacana

Phil.AJ512773

––

––

–tarapacana

AJ512778

Potaninia

––

mongolica

Maxim

Nor-

lindhandAhti

10384(S)

AM286742

––

––

–mongolica

Nor-

lindhandAhti

10384(S)

AM286742

Potentilla

indica(A

n-

drews)

T.Wolf

DQ88374

–reptansL.

U90784

anserinaL.

Potter

970309-

02(D

AV)

AF196916

–anserina

AF288113

––

reptans

AJ512241


Table

2.(C

ontinued)

Poteridium

––

annuum

(Nutt.ex

Hook.)Spach

AY635032

––

––

–annuum

AY634766

Poterium

––

sanguisorbaL.

AY634772

––

–sp.DQ851541

–sanguisorba

AY635038

Prinsepia

uniflora

Batal.

DQ88375

sinensis(O

liv.)

Oliv.ex

Bean

AF285990

sinensisAF318751

sinensisHar-

vard

Univ.

AF196919

sinensisHar-

vard

Univ.

DQ851215

sinensis

AF288114

sinensis

DQ851542

uniflora

U06819

sinensis

AF348558

Prunus

virginianaL.

DQ88377

virginiana

AF285991

AF500453

laurocerasusL.

AF318724

––

laurocerasus

AF288116

carolinana(P.

Mill.)Ait.

DQ851544

laurocerasus

U06809

laurocerasus

AF348559

Prunus

dulcis(M

ill.)D.

A.Webb

DQ88376

persica

(L.)Batsch

AF318741

dulcis

‘Padre’

Bortiri68

(DAV)

AF196923

dulcis

‘Padre’

Bortiri68

(DAV)

DQ851216

dulcis

AF288115

dulcisBortiri68

(DAV)

DQ851543

persica

AF206813

persica

AF348560

Pseudocydonia

–sinensis

(Thouin)

Schneider

AF500454

DQ874911

sinensisU16201

––

sinensis

DQ860471

sinensis

DQ851545

–sinensis

DQ863243

Purshia

tridentata

DC.

DQ88378

tridentata

DQ904405

tridentata

Potter

970831-02(D

AV)

DQ88357

tridentata

Pot-

ter970831-02

(DAV)

AF196927

–tridentata

AF288119

tridentata

Pot-

ter970831-02

(DAV)

DQ851546

tridentata

U06821

tridentata

AF348562

Pygeum

––

––

–topengiiMerr.

Wen

5813(F)

DQ851230

––

–

Pyracantha

–coccinea

Roe-

mer

AF500455-

AF500456

coccinea

DQ811772

––

coccinea

DQ860472

coccinea

DQ851547

–coccinea

DQ863244

Pyrus

communis

L.

AF195622

calleryana

Decne.

AF500457-

AF500459

DQ874900

DQ875905

calleryanaU16202

–caucasica

Fed.

DQ851218

calleryana

DQ860473

communis

DQ851548

–calleryana

DQ863245

Rhamnus

catharticaL.-

AJ235979

cathartica

AF285992

cathartica

AY626436

californica

(Eschsch.)A.

GrayUCD

Arb.A93.0177

AF196933

californica

UCD

Arb.

A93.0177

DQ851196

californica

AF288121

cathartica

DQ851549

cathartica

L13189

californica

AF348565

Rhaphiolepis

–indica(L.)

Lindley

AF500460-

AF500462

indicaU16203

––

indica

DQ860474

indica

DQ851550

–indica

DQ863246

Rhodotypos

scandens

(Thunb.)Mak.

DQ88379

scandens

DQ904406

scandensUC

Bot.

Gard.86.0616

AY177141

scandensUC

Bot.Gard.

86.0616

AF196936

scandensUC

Bot.Gard.

86.0616

DQ851219

scandens

AF288122

–scandens

U06823

scandens

AF348566

Rosa

hybridaL.

X66773

multiflora

Thunb.

AF285993

majalisHerrm

.U90801

––

californica

Cham.&

Schlecht.

AF288123

blandaAit.

DQ851551

woodsiiLindl.

U06824

majalis

AJ512229


Rubus

idaeusL.

DQ88380

odoratusL.

AF285994

chamaem

orus

L.U90803

––

ursinusCham.

&Schlecht.

AF288124

idaeus

DQ851552

idaeusU06825

chamaem

orus

AJ416464

Sanguisorba

––

officinalisL.

AY635041

––

––

officinalis

AY395560

officinalis

AJ416465

Sibbaldia

––

procumbensL.

U90820,

U90821

––

––

–procumbens

AJ512235

Sibbaldianthe

––

bifurca(L.)

Kurtto

&T.

Eriksson

U90786

––

––

–bifurca

AJ512224

Sieversia

–pentapetala

(L.)

Greene

AJ871484T.

Eriksson749

(SBT)

AM116872

pentapetala

AJ302359

––

––

–pentapetala

AJ297345

Sorbaria

–sorbifolia(L.)

A.Br.

AF500463-

AF500464,

DQ904407

sorbifolia

AF318758

sorbifoliaUC

Bot.Gard.

83.0529

AF196947

–sorbifolia

AF288125

sorbifolia

DQ851553

arborea

Schneid.

U06826

sorbifolia

AF348569

Sorbus

–americana

Marsh.

AF500465-

AF500468

DQ874905

aucupariaL.

U16204

–californica

GreeneOhs.n.

(DAV)

DQ851220

californica

AF288126

americana

DQ851554

scopulina

GreeneU06827

americana

DQ863247

Spenceria

––

––

––

sp.DQ851555

–ramalanaTri-

men

DQ88383

Spiraea

XbumaldaBur-

venich.U42801

trilobata

L.

DQ904408

densiflora

Nutt.

Potter

970619-

02(D

AV)

DQ88362

densiflora

Pot-

ter970619-02

(DAV)

AF196949

densiflora

Pot-

ter970619-02

(DAV)

DQ851222

densiflora

AF288127

cantoniensis

Lour.UCD

Arb.DQ851556

Xvanhouttei

(Briot)

Zabel

L11206

densiflora

AF348571

Spiraeanthus

––

––

––

schrenckianus

(Fisch.&

Mey.)

Maxim

.DQ851557

––

Stranvaesia

–davidiana

Decne.

AF500470–

AF500473

––

–davidiana

DQ860476

davidiana

DQ851558

–davidiana

DQ863248

Torm

inalis

–clusii(R

oem

er)

Robertson&

Phipps

AF500474–

AF500475

clusii

DQ811773

––

clusii

DQ860477

clusii

DQ851559

–clusii

DQ863249

Vauquelinia

californica

(Torr.)Sarg.

DQ88382

californica

AF285995-

AF285998

californica

AY555316

californica

UCD

Arbor.

A77.0200

AF196954

californica

UCD

Arbor.

A77.0200

DQ851223

californica

AF288129

californica

DQ851560

corymbosa

Correa

U06829

californica

AF348573


(PPO9: TCCACAACTCCTGGCTCTT andPPO10: TTCTCGTTGTAAAACAAGAA) werealso designed. PCR amplification and sequencingfollowed the methods described above for pgip.

trnL-F: Amplification and sequencing used thec-f primer pair of Taberlet et al. (1991). Methodsare described in Eriksson et al. (2003). Sequencefragments were proof-read and assembled using theStaden Package (Staden 1996).

gbssi: New sequences were obtained usingmethods described by Evans et al. (2000) orSmedmark et al. (2003)

Data Analyses. Sequences of all regions werealigned manually, in some cases using Se-Al(Rambaut 1996), and/or ClustalX (Thompsonet al. 1997). For pgip and ppo, nucleotides werealigned to amino acid alignments using DAMBE(Xia and Xie 2001). Introns (gbssi1, gbssi2, andsome pgip sequences) and ambiguously alignedregions were excluded from all subsequent analy-ses.

Each of the ten loci was analyzed separately forall taxa for which data were available. A combineddata matrix comprising all ten loci and 91 taxa,representing 88 genera of Rosaceae, with CeanothusL. and Rhamnus L. (Rhamnaceae) included asoutgroups (Table 2), was assembled by combiningsequences of members of the same genus, and,when possible, the same species from all of thedifferent regions. We sought to include one speciesfrom most currently recognized genera of Rosa-ceae. Based on the results of previous phylogeneticstudies (Lee and Wen 2001; Bortiri et al. 2001,2002; Shaw and Small 2004), two composite taxawere used to represent the diversity within the largegenus Prunus; one corresponding to the Amygda-lus/Armeniaca/Prunus (peach-almond/apricot/plum) clade and the other to the Cerasus/Lauro-cerasus/Padus (cherry/laurel-cherry) clade. In caseswhere recent phylogenetic evidence strongly sup-ports inclusion of one genus within another, weincluded only one species to represent both. Forexample, we did not include separate representa-tives for Stephanandra and Neillia because recentevidence showed that the former genus is nestedwithin the latter and the two have now been merged(Oh 2006). In two other cases, a genus wasrepresented even though it had already beencombined with another, because no molecularphylogenetic study in support has yet been pub-lished. One such case pertains to Pygeum, which

was transferred to Prunus by Kalkman (1965), theother to Cowania, which was transferred to Purshiaby Henrickson (1986).

In Rosoideae, several genera were lumped intoPotentilla (Duchesnea, Horkelia, and Ivesia) basedon previous analyses (Eriksson et al. 1998, 2003),and into Geum (Novosieversia, Erythrocoma, Onco-stylus, Acomastylis, and Taihangia; see Smedmark,2006). Material was not available for Stellariopsis,Comarella, and Purpusia, but according to pre-liminary study of morphology they are expected tobe included in Potentilla. Fragaria is not combinedwith Potentilla, as suggested by Mabberley (2002),because it would make Potentilla polyphyletic.Generic delimitations in Sanguisorbeae follow Kerr(2004).

For three genera of Spiraeeae (Table 1), mate-rial was not available, but Potter et al. (2007)support inclusion of both Sibiraea and Xerospiraeain the tribe. No data at all were available for themonotypic Korean genus Pentactina.

For cloned sequences (gbssi1, gbssi2, pgip, andppo), one clone per taxon was selected randomly.Missing data were coded as necessary for particularlocus-genus combinations. Sequence alignments areavailable from the corresponding author.

In addition to simultaneous analyses of all tenloci, analyses of various partitions of the total dataset were also conducted (Table 3). Because of somequestionable results of analyses of pgip and ppo (seeResults), analyses were run excluding those twoloci. The four chloroplast loci were analyzed incombination, as were the six nuclear loci, and thefour nuclear loci other than pgip and ppo. In thelast two cases, five taxa (Coleogyne, Cowania,Kelseya, Pygeum, Spenceria, and Spiraeanthus),for which there were no data from any nuclearlocus, were omitted.

Phylogenetic analysis of the data employingmaximum parsimony was implemented in theUNIX version of PAUP* 4.0 b10 (Swofford 2002)using heuristic searches and 1,000 replicates ofrandom taxon addition with TBR branch-swap-ping, MulTrees in effect, and maxtrees allowed toincrease automatically as necessary for most datasets. In order to expedite the search on the ITS dataset, a maximum of 100 trees were saved perreplicate. In four cases (matK, ndhF, trnL-trnF,and the combined chloroplast loci), because of thelarge number of most parsimonious trees(>600,000) recovered on the first replicate in


preliminary analyses, an alternative search strategywas ultimately used to maximize the chances thatwe had indeed recovered the shortest possible trees:20,000 replicates of random addition sequence,saving a single tree per replicate. All positions wereweighted equally; gaps were treated as missingvalues. Branch support was assessed using 10,000parsimony bootstrap replicates, each with a singlerandom addition sequence replicate and TBRbranch-swapping saving a single tree per replicate.

Bayesian analyses, using models of sequenceevolution for each data partition selected in MrAIC(Nylander 2005), were implemented in MrBayes3.1.1 (Huelsenbeck and Ronquist 2001). For eachdata set and combination of data sets, doubleanalyses were run with four chains for 1,000,000generations, sampling every 100 generations. Burn-in was set to 100,000 generations, except for thetrnL-trnF data set where burn-in was set to 200,000generations. The sampled trees from both analyseswere pooled and majority-rule consensus trees wereconstructed from the remaining 18,000 (16,000 inthe case of trnL-trnF) trees to estimate Bayesianclade credibility values.

Non-molecular character states were scoredaccording to our own observations and publishedreports (Table 4). A primary objective of thisproject was to use our phylogenies to study theevolution of fruits, for which we needed detailedinformation on mature fruit characteristics. Suffi-ciently detailed data for some taxa (i.e. Pyrinae)were available from the literature, but for manygenera more detailed information was necessary.This information was produced by obtainingmature fruiting material, dissecting the fruits, andrecording detailed observations on their structure.MacClade 4.06 (Maddison and Maddison 2003)was used to map non-molecular character statesand geographic distributions by continent (Hutch-inson 1964) onto one of the most parsimonioustrees obtained from the phylogenetic analyses ofmolecular data.

Taxonomy. Our primary criterion for formaltaxonomic recognition of groups was strong sup-port by the data. In order to be given formalrecognition, a clade had to meet all of the followingspecific criteria: 1) Congruence among data sets:Monophyly of the group must not be strongly(95% or greater parsimony bootstrap support and/or 95% or greater Bayesian clade credibility)contradicted by any analysis of a single data

partition or any combination of partitions. 2)Robustness: Monophyly of the group must besupported with at least 85% parsimony bootstrapsupport and 95% Bayesian clade credibility in thecombined analysis of all data sets. 3) Consistencywith previous classifications: As much as possiblewithin the constraints of recognizing only puta-tively monophyletic groups, we sought to make ourclassification maximally consistent with previousclassifications, in terms of the numbers and cir-cumscriptions of subfamilies and tribes.

Names were selected for subfamilies, tribes,and subtribes following the rules of the Interna-tional Code of Botanical Nomenclature (ICBN,Greuter et al. 2000). Authorship, priority, and validpublication of names were determined by examin-ing original publications and by consulting severalsources (Kalkman 2004, Reveal 2004, Pankhurst2005, International Plant Names Index 2006).

Results

The total number of characters, number ofparsimony informative characters, number oftaxa, number and statistics of most parsimo-nious trees recovered, and model of sequenceevolution selected for each of our data parti-tions are presented in Table 3, while thesignificant clades supported by various analy-ses are summarized in Table 5. Clades are heredesignated using the taxonomic names listed incolumn 1 of Table 1.

Phylogenetic analyses of the nuclear genespgip and ppo both produced results (notshown) that were inconsistent in some wayswith the majority of the other data and witheach other and that are therefore consideredanomalous. In the case of pgip, parsimonyanalyses placed Rosoideae sister to Os-maronieae with moderate (71% parsimonybootstrap) support and Spiraeeae sister to thatclade with weak (34% parsimony bootstrap)support; neither of these relationships wassupported by Bayesian analysis. The ppo dataprovided strong (75% parsimony bootstrap,100% Bayesian clade credibility) support for asister relationship between Osmaronieae andSpiraeeae, in conflict with the chloroplast data,


Table

3.Characteristics

ofmoleculardata

sets

included

inthisstudy

Region

Number

oftaxa

(alone/

combined)

Aligned

length

Number

Included

Number

Inform

ative

Model

Number

MPT

Length

CI(*)

RI

matK

64/64

1576

1558

346

GTR-G

>600,000

1170

.6855(.5671)

.8172

ndhF

66/64

1106

1106

298

GTR-G

>600,000

1165

.5717(.4893)

.7796

rbcL

50/43

1547

1436

207

GTR-I-G

8731

.5267(.4401)

.7136

trnL-trnF

85/85

1452

1295

333

GTR-G

>600,000

1296

.6451(.5486)

.8600

18S

28/28

1654

1654

63

GTR-I-G

1134

238

.6807(.5097)

.6530

gbssi1

46/46

941

941

277

GTR-I-G

462

1220

.5336(.4422)

.6711

gbssi2

43/43

941

941

282

GTR-G

18,456

1155

.5688(.4813)

.6862

ITS

81/80

793

702

368

GTR-G

1600

2624

.3605(.3151)

.5994

pgip

31/29

841

841

370

HKY-G

21616

.5291(.4697)

.6069

ppo

28/25

1416

1416

614

GTR-G

42358

.5356(.4959)

.6861

Allpartitions

91

12,267

11,890

3084

GTR-G

1214

13631

.5246(.4446)

.6872

Allbutpgip,ppo

91

10,010

9633

2131

GTR-G

226

9682

.5225(.4302)

.7112

chloroplast

only

91

5681

5395

1141

GTR-G

>600,000

4312

.6143(.5100)

.8008

nuclearonly

85

6586

6495

1943

GTR-G

15,389

9226

.4880(.4225)

.6180

nuclearexceptpgip,ppo

85

4329

4238

990

HKY-I-G

1824

5304

.4554(.3782)

.6220

*excludingautapomorphies


Table

4.Non-m

olecularcharactersofparticularphylogenetic

interest

intheRosaceae.

Characters1-12are

mapped

inFig.2;character

13is

mapped

inFig.3,andcharacter

14ismapped

inFig.4

Character

States

Description

References

1.Ovary

connation

0absent

Hutchinson1964;Robertson,

Phipps,andRohrer1991

1present

2.Style

connation

0absent


Phipps,andRohrer1991;

EvansandDickinson1999a,

1999b;EvansandDickinson2005

1present

3.Enlarged

receptacle

0present

Hutchinson1964

1absent

4.Pistilnumber

0one


Phipps,andRohrer1991;

Rohrer,Robertson,and

Phipps1994

1one-five

2>five

5.Ovary-hypanthium

adnation

0no


Phipps,andRohrer1991;Rohrer,

Robertson,andPhipps1994

1yes

6.Nitrogen

fixation

0present

BensonandSilvester1993

1absent

7.Sorbitolproduction

0absent

Wallaart

1980

1trace

<1.0%

ofdry

leaves

2present>1.0%

ofdry

leaves


Table

4.(C

ontinued)

Character

States

Description

References

8.Base

chromosome

number

07

Roitmanet

al.1974,Missouri

BotanicalGarden

2005

18

29

312

415

517

9.Leafmorphology

0compound

Hutchinson1964

1simple

10Stipules

0present

Hutchinson1964

1absent

2deciduous

11.Gymnosporangium

host

0no

Savile1979;Farr

1989;

Farr

etal.2005

1yes

12.Phragmidium

host

0no

Savile1979;Farr

1989;

Farr

etal.2005

1yes

13.Ovule

number/locule

andposition

withrespect

toeach

other

0one

Hutchinson1964;Sterling1964,1965a,1965b,

1965c,

1966;Robertson,Phipps,andRohrer1991;

Evans1999;EvansandDickinson1999b;

EvansandDickinson2005

1tw

o/collateral

2tw

o/superposed

3>tw

o/clustered

4>2/files

14.Fruittype

0pome

Hutchinson1969;Spjut1994

1polypyrenousdrupe

2drupe

3drupetum

4achene

5achenetum

6follicetum

7coccetum

8nucculanium


which strongly supported monophyly of Ker-riodae, the clade comprised of Osmaronieaeand Kerrieae. Including pgip and ppo in thecombined data set favored, with strong sup-port (93% parsimony bootstrap and 100%Bayesian clade credibility) the resolution ob-tained with ppo alone (Table 5). Similarly, thesister relationship between Lyonothamnus andthe rest of Spiraeoideae, strongly supported bythe chloroplast data, was lost when pgip andppo were included in the combined analysis.These anomalous results led us to question thereliability of the pgip and ppo results, at leastwith respect to the relationships mentioned.We therefore constructed trees based on a datamatrix consisting of all sequences except pgipand ppo. The strict consensus tree resultingfrom parsimony analysis of all sequencesexcept pgip and ppo is shown in Figure 1.The distributions of states of selected non-molecular characters of interest (Table 4) weremapped onto one of the most parsimonioustrees from this analysis (Figs. 2–4), revealingvarying degrees of homoplasy in non-molecu-lar characters with respect to hypotheses ofphylogenetic relationship based on moleculardata.

The results of our phylogenetic analyses,combined with our criteria for taxonomicrecognition of clades (see Materials and meth-ods), have led us to propose the classificationpresented in Table 1 and described in furtherdetail below (see Discussion). We recognizethree subfamilies: Rosoideae, Dryadoideae,and Spiraeoideae. Within Rosoideae, we rec-ognize one supertribe, three tribes, and threesubtribes, and within Spiraeoideae we recog-nize two supertribes, seven tribes, and onesubtribe.

Discussion

Phylogenetic resolution. Phylogenetic analysesof combined sequence data from nuclear andchloroplast loci (Table 3) provided strongsupport for all of the infrafamilial taxa recog-nized here (Table 1). All of these groups werealso supported by the chloroplast data alone,

but not all were supported by the nuclear locialone (Table 5). Furthermore, the signal in thepgip and ppo data differed enough from thechloroplast loci with respect to the resolutionof relationships among tribes within Spiraeoi-deae so as to result in conflicting topologies ofthe trees produced from the data set includingall loci and the one including all loci minuspgip and ppo. In particular, whereas in treesresulting from both the combined cpDNAdata set and the combined chloroplast andnuclear data set excluding pgip and ppo,Lyonothamnus was sister to all other Spiraeoi-deae and monophyly of Kerriodae (Os-maronieae plus Kerrieae) was stronglysupported, neither of those relationships wassupported in the combined data set includingall loci.

In the case of both pgip and ppo, we do nothave a definitive explanation for the anoma-lous results but we cannot rule out the possi-bility of incorrect orthology assessment(suggested by some strong conflicts with theother data sets) and/or long branch attraction(suggested by some differences between resultsof parsimony and Bayesian analyses). Becausewe had concerns about the validity of some ofthe relationships resolved by pgip and ppodata, we chose to use the topology supportedby the data set excluding pgip and ppo foroptimization of non-molecular characters. Onthe other hand, inclusion of the pgip and ppodata did not violate any of the criteria fortaxonomic recognition of any group to whichwe have given such recognition. It is alsonoteworthy that the nuclear loci alone pro-vided generally weak and/or conflicting reso-lutions among the tribes in Spiraeeae(Table 5). This could be taken as suggestiveof hybridization among the ancestors of theselineages, but it is difficult to draw any definitiveconclusions because the taxon sampling wasdifferent for each locus.

The combined data set of eight regions and88 genera of Rosaceae is missing almost 40%of the data. The average number of generegions for which sequences are available(Table 2) is 4.9 (± 2.2). To determine whether


Fig. 1. Strict consensus of 226 most parsimonious trees (l = 9,682, ci = 0.5225 (0.4302 excludingautapomorphies), ri = 0.7112) from phylogenetic analysis of all data partitions except pgip and ppo. Bootstrap(above branches) and Bayesian clade credibility (below branches, in italics) support values are indicated. Arrowsare used to indicate groups that were supported by the Bayesian analysis but were not recovered in the strictconsensus tree. (In the Bayesian tree, the branching order within Spiraeoideae was: Lyonothamnus; Neillieae;(the branch leading to the remainder of the subfamily supported with 68% clade credibility), Kerriodae; (thebranch leading to the remainder of the subfamily supported with 100% clade credibility), Amygdaleae; the restof the subfamily)


Fig. 2. Hypothesis for character evolution of 12 morphological, chemical, and fungal host associations.Character states were mapped onto one of the 226 most parsimonious trees. Characters and states correspondto those listed 1–12 in Table 4. Character state changes along branches are labelled as follows: black boxes areapomorphies (syn-, aut-); white boxes are reversals; gray boxes are unresolved. Character states were optimizedin MacClade using DELTRAN


AcaenaMargyricarpusPolylepisCliffortiaSanguisorbaPoteridiumPoteriumAgrimoniaAremoniaHageniaLeucosideaSpenceriaAlchemillaComarumSibbaldiaSibbaldiantheChamaerhodosDasiphoraPotaniniaDrymocallisFragariaPotentillaRosaFallugiaGeumSieversiaRubusFilipendulaAdenostomaChamaebatiariaSorbariaSpiraeanthusAmelanchierPeraphyllumMalacomelesCrataegusMespilusAriaChamaemespilus

TorminalisCormusPyracanthaAroniaDocyniopsisEriolobusDichotomanthesChaenomelesOsteomelesChamaemelesMalusCotoneasterEriobotryaRhaphiolepisHeteromelesPyrusStranvaesiaCydoniaPhotiniaPseudocydoniaSorbusVauqueliniaKageneckiaLindleyaGilleniaAruncusLuetkeaHolodiscusKelseyaPetrophytonSpiraeaColeogyneKerriaNeviusiaRhodotyposExochordaOemleriaPrinsepiaMaddeniaPygeumPrunus lPrunus dNeilliaPhysocarpusLyonothamnusCercocarpusChamaebatiaCowaniaPurshiaDryasCeanothusRhamnus

ovule #/loculeunordered

one

two \ collateral

two \ superposed

> two \ clustered

> two \ files

polymorphic

uncertain

Fig. 3. Hypothesis for evolution of ovule number and position with ovary locule (Character 13 in Table 4).Character states were mapped onto one of 226 most parsimonious trees (identical to the one used in Fig. 2).Character states were optimized in MacClade using DELTRAN


AcaenaMargyricarpusPolylepisCliffortiaSanguisorbaPoteridiumPoteriumAgrimoniaAremoniaHageniaLeucosideaSpenceriaAlchemillaComarumSibbaldiaSibbaldiantheChamaerhodosDasiphoraPotaniniaDrymocallisFragariaPotentillaRosaFallugiaGeumSieversiaRubusFilipendulaAdenostomaChamaebatiariaSorbariaSpiraeanthusAmelanchierPeraphyllumMalacomelesCrataegusMespilusAriaChamaemespilusTorminalisCormusPyracanthaAroniaDocyniopsisEriolobusDichotomanthesChaenomelesOsteomelesChamaemelesMalusCotoneasterEriobotryaRhaphiolepisHeteromelesPyrusStranvaesiaCydoniaPhotiniaPseudocydoniaSorbusVauqueliniaKageneckiaLindleyaGilleniaAruncusLuetkeaHolodiscusKelseyaPetrophytonSpiraeaColeogyneKerriaNeviusiaRhodotyposExochordaOemleriaPrinsepiaMaddeniaPygeumPrunus lPrunus dNeilliaPhysocarpusLyonothamnusCercocarpusChamaebatiaCowaniaPurshiaDryasCeanothusRhamnus

fruitunordered

pome

polyprenous drupe

drupedrupetum

achene

achenetum

follicetum

coccetum

nuculanium

polymorphic

equivocal

Fig. 4. Hypothesis for evolution of Rosaceae fruit type (Character 14 in Table 4). Character states weremapped onto one of 226 most parsimonious trees (identical to the one used in Fig. 2). Character states followSpjut (1994) and were optimized in MacClade using DELTRAN


Table

5.Supportvalues

(parsim

onybootstrap/Bayesiancladecredibility)forvariousclades

byvariousdata

partitions.Only

clades

withatleast

85%

bootstrapor95%

Bayesiancladecredibilitysupport

from

atleast

onedata

partitionare

included.Thecompositionoftheclades

varies

amongthedifferentanalysesdueto

differencesin

taxonsamplingamongthedifferentpartitions(see

Tables2and3).Thedesignation‘‘na’’means

therelevanttaxawerenotincluded

totestsupportforthecladein

question;‘‘–"meansthecladewasnotcompatiblewiththe50%

majority-rule

bootstraptree

orthatitwassupported

withless

than50%

Bayesiancladecredibility;‘‘*’’meansthatitwascompatible

withthe50%

majority-

rule

bootstraptree

butwasnotrecovered

inthestrict

consensustree

(parsim

ony)forthedata

setin

question;‘‘**’’meansthatit

wasnot

compatiblewiththe50%

majority-rulebootstraptree

butitwasrecovered

inthestrict

consensustree

(parsim

ony)forthedata

setin

question.In

thecase

ofgbssi2,nooutgroupswereincluded

intheanalysis;treesweretherefore

rootedbetweenRosoideaeandtherestofthefamily,consistent

withtheresultsfrom

most

oftheother

data

sets

Clade

18S

gbssi1

gbssi2

ITS

pgip

ppo

matk

ndhF

rbcL

trnL-trnF

All

nuclear

Nuclear

except

pgip,

ppo

Chloro-plast

only

All

Loci

All

except

pgip

andppo

1.Rosoideae

73/97

96/100

100/100

73/100

100/100

100/100

100/100

100/100

100/100

90/98

90

89/100

99/100

100/100

100/100

2.Dryadoideae

86/100

na

100/100

100/100

95/100

100/100

94/100

99/100

99/100

100/100

100

100/100

100/100

100/100

100/100

3.Spiraeoideae

–/–

49*/90

68/96

44/79

–/–

73/100

94/100

51/100

30/52

64/98

94

87/100

99/100

100/100

100/100

4.Colurieae

na

98/100

97/100

88/100

na

na

na

50*/100

98/100

100/98

100

100/100

99/100

100/100

100/100

5.Potentilleae

–/–

na

na

–/–

na

na

93/100

75/100

99/100

90/100

––/–

99/100

99/100

91/100

6.Sanguisorbeae

na

na

na

23*/–

na

na

na

99/100

99/100

100/100

28*

32*/–

100/100

100/100

100/100

6a.Sanguisorbinae

na

na

na

32*/94

na

na

na

75/73

na

100/100

42

35*/98

100/100

100/100

100/100

6b.Agrimoniinae

na

na

na

99/100

na

na

na

na

na

98/100

99

99/100

98/100

98/100

98/100

7.Amygdaleae

92/100

na

na

97/100

100/100

100/100

100/100

100/100

98/100

100/100

98

99/100

100/100

100/100

100/100

8.Osm

aronieae

100/100

38*/58

100/100

100/100

100/100

100/100

100/100

100/100

99/100

100/100

100

100/100

100/100

100/100

100/100

9.Kerrieae

–/–

42*/100

na

–/–

56*/97

na

99/100

100/100

83/100

77/99

54

–/82

100/100

100/100

98/100

10.Neillieae

57*/100

99/99

na

100/100

100/100

100/100

100/100

100/100

76/100

100/100

100

100/100

100/100

100/100

100/100

11.Pyrodae

–/–

96/100

100/100

77/100

100/100

100/100

100/100

100/100

100/100

100/98

99

99/85

100/100

100/100

100/100

11a.Pyreae

–/–

74/100

99/100

–/–

79/99

99/100

65/85

76/74

76/66

92/98

95

92/85

100/100

100/100

100/100

11b.Pyrinae

57*/69

84/100

83/100

48/94

100/100

100/100

70/100

24*/92

55/89

93/98

95

97/89

99/100

100/100

100/100

12.Sorbarieae

70*/98

100/100

100/100

100/100

100/100

100/100

100/100

100/100

95/100

100/100

100

99/100

100/100

100/100

100/100

13.Spiraeeae

93/100

na

96/100

95/100

100/100

100/100

100/100

100/100

97/100

100/100

100

90/99

100/100

100/100

100/100

1plus2

–/–

–/–

na(root)

–/–

–/–

–/–

–/78

–/–

–/64

–/–

––/–

–/–

–/–

–/–

2plus3

44*/79

38*/51

na(root)

52/–

–/–

71/99

46/–

68/99

35/–

64/98

88

67/84

89/90

98/100

94/96

1plus3

–/–

–/–

na(root)

–/–

55/–

–/–

–/–

–/–

–/–

–/–

––/–

–/–

–/–

–/–

Kerriodae(8

plus9)

–/–

–/–

na

7/–

–/–

–/–

57/100

39*/80

–/–

49/74

–31*/83

94/100

–/–

88/100

1exceptFilipendula

–/–

56*/–

96/100

–/–

na

na

na

na

86/70

100/98

–46/91

100/100

99/100

99/100

1exceptFilipendula

andRubus

–/–

79/100

97/100

–/–

na

na

na

–/–

–/–

79/–

––/–

–/–

50/–

42/–

1exceptFilipendula,

Rubus,and4

na

na

na

–/–

na

na

na

36/73

90/100

98/100

51*

53/100

99/100

100/100

100/100

Rosa

plus5

–/–

92/100

na

–/–

na

na

99/100

47/85

82/87

–/–

22

–/–

80/97

71/87.5

79/83


our results in analysis of the data set of 88genera were affected by missing data, weassembled a data set for all 10 regions withtwo exemplars each from Rosoideae, Dryadoi-deae, Osmaronieae, Kerrieae, Neillieae, Pru-nus, Pyreae, Sorbarieae, and Spiraeeae as wellas Lyonothamnus, Results of parsimony anal-yses of this exemplar data set (not shown)agree with the analyses of the 88-genus data setin strongly supporting these major groups aswell as the Spiraeoideae as we circumscribe itand in uncertainty about relationships amongthe three subfamilies and among most tribes ofSpiraeoideae. Hence we are confident thatmissing data do not affect our conclusions,consistent with the simulation study by Wiens(2003).

Our results agree with all previous phylo-genetic analyses of Rosaceae in providing littleresolution along the backbone of the Rosaceaephylogenetic tree. Resolution is especially pooramong tribes of Spiraeoideae, where variousgroupings received generally weak or moderatesupport, depending on the data set andmethod of analysis (Table 5). Most of theresolution present in Fig. 1 is provided by ourchloroplast loci, but it is important to note thatthe chloroplast loci were also more thoroughlysampled than the nuclear loci. Most of ourdata support a sister relationship betweenRosoideae and the other two subfamilies, butthere is also some support for a sister relation-ship between Rosoideae and Dryadoideae(Table 5). Both rapid evolutionary radiationof lineages and reticulations among the ances-tors of those lineages are possible explanationsfor these patterns. These processes have beenimplicated in the evolution of the Pyreae(Campbell et al. 2007).

Patterns of character evolution. With thecaveat that relationships among Rosales andother members of the nitrogen-fixing clade ofeurosids I remain poorly resolved (AngiospermPhylogeny Group 2003), our parsimony recon-struction analyses support the following ances-tral states within Rosaceae: shrubs with alter-nate simple leaves, sorbitol absent, stipulespresent, stamens numerous (>10), pistils 1–5,3

exceptLyonothamnus

–/–

na

–/–

–/–

–/–

–/–

85/100

33/99

–/–

82/98

––/–

98/100

–/–

79/100

3except7

–/–

–/–

–/–

–/–

–/–

–/99

–/–

–/–

–/–

–/–

––/–

–/–

–/–

–/–

3except10

–/–

12*/74

na

16/86

–/–

36/–

–/–

–/–

–/–

–/–

41

36/100

–/–

42/64and<50

–/–

7,11,12,and13

–/–

–/–

–/–

–/93

–/–

–/–

37/99

–/–

–/–

–**/98

––/–

65/100

–/–

–/100

11,12,and13

–/–

–/–

–/–

54/88

–/–

–/–

–/–

–/–

–/–

–/92

–42/84

–/87

–/–

70/100

Lyonothamnusplus8,9,

12,and13

–/–

na

na

–/–

–/–

72/100

–/–

–/–

–/–

–/–

53

–/–

–/–

46/99.5

–/–

Lyonothamnusplus8,

12,and13

–/–

na

–/–

–/–

–/–

52/100

–/–

–/–

–/–

–/–

––/–

–/

–/–

–/–

Lyonothamnusplus9

and12

–/–

na

–/–

–/–

–/–

–/–

–/–

–/–

–/–

–/–

38

–/–

–/–

34/99.5

–/–

8plus13

–/–

na

–/–

–/–

–/–

75/100

–/–

–/–

–/–

–/–

77

–/–

–/–

93/100

–/–

9plus12

–/–

26*/95

na

–/–

–/–

–/–

–/–

–/–

–/–

–/–

35

–/–

–/–

–/–

–/–

9plus10

–/–

–/–

na

–/–

30*/95

–/–

–/–

–/–

–/–

–/–

––/–

–/–

–/–

–/–


hypanthium free from ovaries, ovaries sepa-rate, styles free, one ovule per locule, and fruitan achenetum or follicetum. The ancestral basechromosome number for the family is either 7or 9. Each of the following character statesevolved independently two or more timeswithin the family (Fig. 2): trees and herbs,compound leaves, loss of stipules (severaltimes in Spiraeoideae), base chromosomenumber x = 8 (once in Rosoideae and severaltimes in Spiraeoideae), ovary connation (sev-eral clades in Spiraeoideae, especially Pyreae),style connation (several derivations withinPyreae), enlarged receptacle (several deriva-tions within Rosoideae), and basal adnation ofthe ovary and hypanthium (several derivationswithin Spiraeoideae). Each of several condi-tions of ovule number and position alsoevolved multiple times (Fig. 3). According toour results, each of the following characterstates may have evolved only once in thefamily: hypanthium adnate to the ovary formore than half of its length (Pyrinae; onereversal), base chromosome number x = 17(15) (Pyreae), and presence of sorbitol as aprimary transport carbohydrate (Dryadoideaeplus Spiraeoideae).

The traditional view of fruit evolutionwithin Rosaceae, as exemplified by the four-subfamily classification (e.g. Schulze-Menz1964) was quite simple, with the derived fruittypes (pome, drupe, achene) originating onceeach from ancestral follicles. In contrast, ourresults agree with other molecular phylogeneticstudies (Morgan et al. 1994, Potter et al. 2002)in suggesting that the evolution of fruit typesin the family has been much more complex(Fig. 4). Some clades are relatively homoge-neous. The Rosoideae and Dryadoideae allhave indehiscent one-seeded fruits, and thePyrinae all have the mature gynoecium en-closed by a fleshy hypanthium (although thereis considerable variation in what the receptacleand hypanthium develop into in Rosoideaeand in what the carpels develop into inPyrinae). The remaining clades are all hetero-geneous with respect to fruit type. For exam-ple, two of the clades that have follicle/

follicetum fruits also contain a genus bearingachene/achenetum fruits: Adenostoma in Sorb-arieae and Holodiscus in Spiraeeae. Three ofthe four clades (Amygdaleae, Kerr-ieae, Osmaronieae, and Pyrinae) containinggenera in which pericarps are drupaceous(having a stony endocarp) also contain generathat have non-drupaceous pericarps: Neviusiain Kerrieae, Exochorda in Osmaronieae, andseveral genera in Pyrinae.

The overall picture of the evolution of fruitsin Rosaceae is not one in which specific combi-nations of characteristics have consistentlyevolved together to yield distinct fruit types(i.e., follicles, achenes, pomes, drupes, etc.), butone in which several different fruit characteris-tics have evolved more or less independently,producing genera and groups of genera thatexhibit different combinations of these charac-teristics. One of several examples is provided byfruits in which the pericarp is drupaceous.As mentioned above, genera with drupaceouspericarps are found in four clades: Pyri-nae, Kerrieae, Osmaronieae, and Amygdaleae.However, the drupaceous pericarps in eachof these clades are accompanied by variouscharacteristics that make them differentfrom one another. For example, the drupa-ceous pericarps in Pyrinae (polyprenous drupesof Crataegus and others) are accompaniedby fleshy hypanthia that enclose the maturegynoecium, which do not occur in the otherthree drupaceous clades. Another example isseen in the drupaceous fruits of Kerrieae, whichdo not have the fleshy mesocarps that are foundin all three of the other drupaceous clades.

Several ecological associations exhibit tax-onomic distributions that appear to correlatewith phylogenetic relationships within Rosa-ceae (Fig. 2). Symbiotic nitrogen fixation, viaassociations with actinomycetes of the genusFrankia, has been observed only in Dryadoi-deae, in which members of all four genera havebeen reported to form nodules. This associa-tion is also found in some members of sevenother families of orders Rosales, Cucurbitales,and Fagales. These three orders, alongwith Fabales, form a subclade, sometimes


designated the nitrogen-fixing clade (APG2003), within the eurosid I clade. Associationwith rust fungi of the genus Gymnosporangiumappears to be restricted to Pyrodae, whileassociation with Phragmidium rusts has beenreported only from members of Rosoideae. Inboth cases, however, sampling has been quitelimited.

The clades resolved within Rosaceae by ouranalyses provide numerous examples ofintriguing biogeographic patterns, includingthe eastern Asia – eastern and western NorthAmerica pattern exemplified by Neillieae (Ohand Potter 2005) and Kerrieae, a central andeastern Asia – western North America patternin Sorbarieae and Osmaronieae, and poten-tially complex patterns involving multiplecontinents in groups such as Rosoideae, Spir-aeeae, Pyrodae, and Amygdaleae. With theexception of Dryas, which has a circumpolardistribution, taxa of Dryadoideae are re-stricted to western North America, andthroughout much of that region the nitrogen-fixing Frankia strains with which they formsymbioses show remarkably little genetic diver-sity (Vanden Heuvel et al. 2004). The phylo-genetic trees generated by our analyses suggesta North American origin for the entire family,each of the three subfamilies, and Pyrodae.However, a series of detailed studies withthorough sampling of species within each tribe,aimed at achieving considerably increasedphylogenetic resolution, will be required totease apart all of the complexities of geo-graphic patterns across the family.

Classification. A new, phylogeneticallybased classification for Rosaceae is proposedbased on the results of our analyses (Table 1),following the criteria listed above (see Mate-rials and Methods).

Some clades received strong support in thecombined analysis but did not meet all three ofthe criteria outlined above; such clades havetherefore not been given taxonomic recogni-tion here. Thus, no name is given to either theclade comprising Dryadoideae plus Spiraeoi-deae or the clade including all members ofSpiraeoideae except Lyonothamnus.

We have chosen to recognize three clades atthe supertribal level: Rosodae, comprising allRosoideae except Filipendula; Kerriodae, com-prising Kerrieae plus Osmaronieae, and Pyro-dae, comprising Pyreae (all with x = 15 or 17)plus Gillenia. The inclusion of supertribesallows us to incorporate greater phylogeneticresolution while maintaining a ranked classifi-cation than would be possible without additionof this rank. In order to minimize the numberof names of different ranks that refer to thesame groups, we chose not to name supergen-eric taxa that would include, based on currentphylogenetic evidence, only one genus. Anexception was made for Prunus, which weplace in tribe Amygdaleae due to the large sizeand diversity of the genus and the limitedsampling to date of species sometimes classi-fied in Maddenia and Pygeum. In Rosoideae,Filipendula is included in the subfamily but notin any tribe, Rosa and Rubus are both includedin Rosodae but not in any tribe, and Potentillais included in Potentilleae but not in anysubtribe, although the remaining genera areplaced in Fragariinae. In Spiraeoideae, Lyon-othamnus is included in the subfamily but isnot in any tribe, Gillenia is included in Pyrodaebut not in any tribe, and Kageneckia, Lindleya,and Vauquelinia are included in Pyreae but notin any subtribe, although the remaining generaare classified in Pyrinae. Our subtribe Pyrinaecorresponds to the long-recognized subfamilyMaloideae (Schulze-Menz 1964) in which thefruit type is generally a pome. Pyrus wasselected as the type genus for its subtribe andtribe in accordance with the ICBN (Greuteret al. 2000, Art. 11.5). The two names availablefor the subtribe are Mespilinae and Pyrinae,both published by Du Mortier (1827) andtherefore of equal priority. Since, to ourknowledge, no one has previously publisheda choice between these two names (Greuter etal. 2000, Art. 11.5), we here select the latter.The tribal name Maleae (Schulze-Menz 1964)was nomenclaturally superfluous when pub-lished since Schulze-Menz listed Sorbeae (Koe-hne 1890) as a synonym; Pyreae (Baillon 1869)has priority over both Sorbeae and Crataegeae


(Koehne 1890). The name Pomeae A. Gray(1842) is invalid because it is a descriptivename, not based on the name of an includedgenus (Greuter et al. 2000, Arts. 18.1, 19.3).The three supertribal names, Rosodae, Ker-riodae, and Pyrodae, are published here for thefirst time.

Taxonomic treatment: infrafamilial classifi-

cation of Rosaceae. In the following descrip-tions, potential synapomorphies are indicatedin bold font. Based on the current results ofour analyses, we complement the traditionalclassification with phylogenetic definitions ofthe hypothesized clades. More detailed discus-sion of the classification of Pyrinae is presentedby Campbell et al. (2007).

Family Rosaceae Juss., Gen. Pl. 334 (1789),

nom. cons.: the clade comprising Rosoideae(cf. below), Dryadoideae (cf. below), andSpiraeoideae (cf. below).

Included taxa: Rosoideae, Dryadoideae,and Spiraeoideae.

Distinctive non-molecular features: Herbs,shrubs, and trees. Cyanogenic glycosides oftenpresent. Sorbitol often present as a transportcarbohydrate. Leaves generally alternate, sim-ple to variously divided or compound. Stipulespresent except where noted. Flowers generallyperfect. Sepals and petals generally 5, stamens

(0–3)5-many, pistils (0)1 – many. Hypanthiumpresent; free from to fully adnate to theovary(ies). Ovaries separate or connate. Stylesfree except in some Pyreae. Fruit an achene,achenetum (multiple achenes from a singleflower), follicetum (multiple follicles from asingle flower), coccetum (multiple carpels froma single flower, separating at maturity andeach dehiscing along two sutures, sometimesdescribed as a capsule), drupe, drupetum(multiple drupelets from a single flower),nuculanium (similar to drupe or drupetumexcept that the mesocarp is not fleshy), po-lyprenous drupe, or pome (descriptive fruitterminology from Spjut 1994). Base chromo-some number x = 7, 8, 9, 15, or 17.

Subfamily Rosoideae (Juss.) Arn., Encycl.

Brit., ed. 7, 5: 107 (1832): the most inclusiveclade containing Rosa (as typified by Rosa

cinnamomea L.), but not Dryadoideae (cf.below) nor Spiraeoideae (cf. below).

Included taxa: Filipendula, Rosodae.Distinctive non-molecular features: Peren-

nial or, rarely, annual herbs, shrubs, or, rarely,trees. Cyanogenic glycosides absent. Sorbitolabsent. Leaves alternate and usually com-

pound. Stipules present. Pistils 1-many. Recep-tacle sometimes enlarged. Hypanthium freefrom ovaries. Ovaries separate. Fruits indehis-cent. Base chromosome number x = 7 (8).

Filipendula Adans.Distinctive non-molecular features: Recep-

tacle enlarged. Pistils 1–5. Fruit an achenetum.Rosodae T. Eriksson, Smedmark, and M. S.

Kerr, supertribus nova Supertribus analysibusphylogeneticis ordinum ADN genorum chlo-roplastorum et nucleorum recognoscitur etvalde sustinetur.

Supertribe Rosodae T. Eriksson, Smed-

mark, and M. S. Kerr: the most inclusive cladecontaining Rosa (as typified by Rosa cinnamo-mea L.), but not Filipendula (as typified byFilipendula vulgaris Moench).

Included taxa: Rosa, Rubus, Sanguisor-beae, Potentilleae, Colurieae.

The supertribe Rosodae exhibits the rangeof character states found in Rosoideae, butexcludes Filipendula.

Rosa L. (including Hulthemia Dumort.)Distinctive non-molecular features: Shrubs.

Pistils numerous. Hypanthium concave, urn-shaped. Fruit an achenetum.

Rubus L. (including Dalibarda L.)Distinctive non-molecular features: Mostly

shrubs. Receptacle enlarged. Pistils numerous.Fruit a drupetum.

Tribe Sanguisorbeae DC., Prodr. 2: 588

(1825): Sanguisorbeae and the enclosed sub-tribes Sanguisorbinae and Agrimoniinae con-form to definitions by Eriksson et al. (2003).

Included taxa: Sanguisorbinae, Agrimonii-nae

Distinctive non-molecular features: Pistils1–5. Fruit an achene or achenetum.

Subtribe Agrimoniinae J. Presl, Wsobecny

Rostl. 1: 502 (1846). Included taxa: AgrimoniaL., Aremonia Neck. ex Nestl., Hagenia J. F.


Gmel., Leucosidea Eckl. & Zeyh., SpenceriaTrimen

Distinctive non-molecular features: Herbs,shrubs (Leucosidea), or trees (Hagenia).

Subtribe Sanguisorbinae Torr. & A. Gray,

Fl. N. Amer. 1: 428 (1840). Included taxa:Cliffortia L., Acaena L., Margyricarpus Ruiz &Pav. (including Tetraglochin Poepp.), PolylepisRuiz & Pav., Poterium L. (including BencomiaWebb & Berthel., Marcetella Svent., Dendrio-poterium Svent., and Sarcopoterium Spach),Poteridium Spach, Sanguisorba L.

Distinctive non-molecular features: Herbs,shrubs (Margyricarpus, some Cliffortia, Polyl-epis, and Poterium), or trees (some Polylepis).

Tribe Potentilleae Sweet, Brit. Fl. Gard. 2:

124 (1825): Potentilleae and the enclosedPotentilla and subtribe Fragariinae conformto definitions by Eriksson et al. (2003).

Included taxa: Potentilla, Fragariinae.Distinctive non-molecular features: Herbs

or shrubs (Dasiphora, Potaninia, and someComarum). Leaves often simple in Alchemilla.Enlarged receptacle common (absent in Al-chemilla and Potaninia). Pistils with lateral tobasal styles. Pistils generally numerous (soli-tary in Potaninia and some Alchemilla). Fruitan achenetum or achene.

Base chromosome number x = 7 (8 inAlchemilla).

Potentilla L. (including Argentina Lam.,Comarella Rydb., Duchesnea Sm., HorkeliaCham. & Schltdl., Horkeliella (Rydb.) Rydb.,Ivesia Torr. & A. Gray, Purpusia Brandegee,and Stellariopsis (Baill.) Rydb.)

Distinctive non-molecular features: noneknown.

Subtribe Fragariinae Torr. & A. Gray, Fl.

N. Amer. 1: 435 (1840). Included taxa:Alchemilla L. (including Aphanes L., Lachem-illa (Focke) Lagerh., and ZygalchemillaRydb.), Chamaerhodos Bunge, Comarum L.(including Farinopsis Chrtek & Sojak), Dasi-phora Raf. (= Pentaphylloides Duhamel),Drymocallis Fourr., Fragaria L., PotaniniaMaxim., Sibbaldianthe Juz. (including Schisto-phyllidium (Juz. ex Fed.) Ikonn.), Sibbaldia L.,Sibbaldiopsis Rydb.

Distinctive non-molecular features: noneknown.

Tribe Colurieae Rydb., N. Amer. Fl. 22: 397

(1913): Colurieae conforms to the definitionin Smedmark and Eriksson (2002).

Included taxa: Geum L. (including Acomasty-lisGreene, ColuriaR. Br.,Novosieversia F. Bolle,Oncostylus (Schltdl.) F. Bolle, Orthurus Juz.,Taihangia T. T. Yu & C. L. Li, and WaldsteniaWilld.), Fallugia Endl., SieversiaWilld.

Distinctive non-molecular features: Pistilsusually numerous. Receptacle often enlarged.Fruit an achenetum or achene.

Subfamilies Dryadoideae plus Spiraeoideae

Base chromosome number x = 8 or higher.

Sorbitol present.

SubfamilyDryadoideaeJuel, Kongl. Svenska

Vetensk. Akad. Handl. n.s. 58: 55 (1918): themost inclusive clade containing Dryas (astypified byDryas octopetala L.), but not Rosoi-deae (cf. above) nor Spiraeoideae (cf. below).

Included taxa: Cercocarpus H. B. & K.,Chamaebatia Benth., Dryas L., Purshia DC.(including Cowania D. Don)

Distinctive non-molecular features: Shrub-lets, shrubs, or small trees. Symbiotic nitrogen

fixation present. Cyanogenic glycosides pres-ent. Sorbitol present in trace amounts. Leavescompound in Chamaebatia, simple in the othergenera. Stipules present. Hypanthium freefrom ovary. Pistils 1 (Cercocarpus, Chamaeba-tia, Purshia) or 4-many (Cowania, Dryas).Fruit an achene or achenetum. Base chromo-some number x = 9.

Subfamily Spiraeoideae C. Agardh, Cl. Pl.

20 (1825): the most inclusive clade containingSpiraea (as typified by Spiraea salicifolia L.),but not Rosoideae (cf. above) nor Dryadoi-deae (cf. above).

Included taxa: Lyonothamnus, Amygda-leae, Neillieae, Sorbarieae, Spiraeeae, Kerrio-dae, Pyrodae

Distinctive non-molecular features: Mostlyshrubs and trees. Sorbitol present in significantamounts. Cyanogenic glycosides generallypresent. Leaves generally simple and alternate.Stipules usually present. Pistils 1–5. Hypan-thium generally free from ovary(ies). Ovaries


generally separate. Fruit a follicetum, achene,achenetum, coccetum, drupe, drupetum, nu-culanium, polyprenous drupe, or pome. Basechromosome number x = 8, 9, 15, or 17.

Lyonothamnus A. GrayDistinctive non-molecular features: Cyano-

genic glycosides absent. Leaves opposite, entireor deeply divided. Stipules deciduous. Hypan-

thium adnate to base of ovaries. Ovaries

connate; hypanthium adnate to base. Fruit afollicetum. Base chromosome number x = 9.

Tribe Amygdaleae Juss., Gen. Pl. 340

(1789): the most inclusive clade containingPrunus amygdalus (L.) Batsch (= Amygdaluscommunis L.) but not Osmaronieae (cf. below),Kerrieae (cf. below), Neillieae (cf. below),Sorbarieae (cf. below), Spiraeeae (cf. below),or Pyrodae (cf. below).

Included taxa: Prunus L. (including Amy-gdalus L., Armeniaca Juss., Cerasus Mill.,Laurocerasus Tourn. ex Duhamel, MaddeniaHook. F. & Thomson, Padus Mill., andPygeum Gaertn.)

Distinctive non-molecular features: Stip-ules deciduous. Pistil solitary. Fruit a drupe.

Base chromosome number x = 8.Tribe Neillieae Maxim., Trudy Imp. S.-

Peterburgsk. Bot. Sada 6: 216 (1879): the mostinclusive clade containing Neillia (as typifiedby Neillia thyrsiflora D. Don) but not Amy-gdaleae (cf. above), Osmaronieae (cf. below),Kerrieae (cf. below), Sorbarieae (cf. below),Spiraeeae (cf. below), or Pyrodae (cf. below).

Included taxa: Neillia D. Don (includingStephanandra Siebold & Zucc.,), Physocarpus(Cambess.) Raf.

Distinctive non-molecular features: Cyano-genic glycosides absent in Physocarpus, nodata for the other genera. Stipules deciduous inPhysocarpus. Ovaries connate. Fruit a follice-tum. Base chromosome number x = 9.

Tribe Sorbarieae Rydb., N. Amer. Fl. 22:

256 (1908): the most inclusive clade contain-ing Sorbaria (as typified by Sorbaria sorbifolia(L.) A. Braun) but not Amygdaleae (cf.above), Osmaronieae (cf. below), Kerrieae(cf. below), Neillieae (cf. above), Spiraeeae(cf. below), or Pyrodae (cf. below).

Included taxa: Adenostoma Hook. & Arn.,Chamaebatiaria Maxim., Sorbaria A. Braun,Spiraeanthus Maxim.

Distinctive non-molecular features: Leavesfascicled or alternate and simple in Adenos-toma, alternate and compound in the remain-ing genera. Ovaries connate (pistil solitary inAdenostoma); hypanthium adnate to base inChamaebatiaria and Sorbaria. Fruit an achene(Adenostoma) or follicetum. Base chromosomenumber x = 9.

Tribe Spiraeeae DC., Prodr. 2: 541 (1825):

the most inclusive clade containing Spiraea (astypified by Spiraea salicifolia L.), but notAmygdaleae (cf. above), Osmaronieae (cf.below), Kerrieae (cf. below), Neillieae (cf.above), Sorbarieae (cf. above), or Pyrodae(cf. below).

Included taxa: Aruncus Adans., HolodiscusMaxim., Kelseya Rydb., Luetkea Bong. (=EriogyniaHook.), Petrophyton Rydb., SibiraeaMaxim., SpiraeaL.,Xerospiraea J. Henrickson.Pentactina Nakai may belong here but has notbeen included in phylogenetic analyses to date.

Distinctive non-molecular features: Herbs(Aruncus) or shrubs, sometimes forming ro-settes.

Stipules absent. Fruit a follicetum or ach-enetum (Holodiscus). Base chromosome num-ber x = 9.

Kerriodae D. Potter, S. H. Oh, and K. R.

Robertson, supertribus nova Supertribus ana-lysibus phylogeneticis ordinum ADN genorumchloroplastorum et nucleorum recognoscitur etvalde sustinetur.

Supertribe Kerriodae D. Potter, S. H. Oh,

and K. R. Robertson: the clade comprisingKerrieae (cf. below) and Osmaronieae (cf.below) if they are sister-groups.

Included taxa: Kerrieae and Osmaronieae.Tribe Osmaronieae Rydb., N. Amer. Fl. 22:

482 (1918): the most inclusive clade contain-ing Oemleria (as typified by Oemleria ceras-iformis (Hook. & Arn.) J. W.Landon) butnot Amygdaleae (cf. above), Kerrieae (cf.below), Neillieae (cf. above), Sorbarieae(cf. above), Spiraeeae (cf. above), or Pyrodae(cf. below).


Included taxa: Exochorda Lindl., OemleriaRchb., Prinsepia Royle (including Plagiosper-mum Oliv.)

Distinctive non-molecular features: Stip-

ules absent in Oemleria, deciduous in the other

genera. Ovaries connate in Exochorda.Fruit a coccetum (Exochorda), drupetum

(Oemleria), or drupe (Prinsepia). Base chromo-

some number x = 8.

Tribe Kerrieae Focke, Nat. Pflanzenfam.

ed. 1, 3: 27 (1888): the most inclusive cladecontaining Kerria (as typified by Kerria japon-ica (L.) DC.) but not Amygdaleae (cf. above),Osmaronieae (cf. above), Neillieae (cf. above),Sorbarieae (cf. above), Spiraeeae (cf. above),or Pyrodae (cf. below).

Included taxa: Coleogyne Torr., Kerria DC.,Neviusia A. Gray, Rhodotypos Siebold & Zucc.

Distinctive non-molecular features: Leavesopposite in Coleogyne and Rhodotypos. Pistilsolitary in Coleogyne. Fruit a nuculanium

(achenetum in Neviusia). Base chromosomenumber x = 9 (8 in Coleogyne).

Pyrodae C. S. Campbell, R. C. Evans, D. R.

Morgan, and T. A. Dickinson, supertribus

nova Supertribus analysibus phylogeneticisordinum ADN genorum chloroplastorum etnucleorum recognoscitur et valde sustinetur.

Supertribe Pyrodae C. S. Campbell, R. C.

Evans, D. R. Morgan, and T. A. Dickinson: themost inclusive clade containing Pyrus (as typ-ifiedbyPyrus communisL.) butnotAmygdaleae(cf. above), Osmaronieae (cf. above), Kerrieae(cf. above), Neillieae (cf. above), Sorbarieae (cf.above), or Spiraeeae (cf. above).

Included taxa: Gillenia Moench, Pyreae.Distinctive non-molecular features: Peren-

nial herbs (Gillenia), trees, or shrubs. Leavescompound in Gillenia, Cormus, Osteomeles,and some Sorbus. Hosts to Phragmidium and

Gymnosporangium rusts; ovaries generally con-nate (separate or single ovaries in Kageneckiaand some members of Pyrinae (Chamaemeles,Cotoneaster, Dichotomanthes, Heteromeles,and Pyracantha)); ovules basal, paired, collat-eral, with funicular obturators.

Tribe Pyreae Baill., Hist. Pl. 1: 442, 475

(1869): the most inclusive clade containing

Pyrus (as typified by Pyrus communis L.) butnot Gillenia (as typified by Gillenia trifoliata(L.) Moench) or Spiraeeae (cf. above)

Included taxa: Kageneckia Ruiz & Pav.,Lindleya H. B. & K., Vauquelinia Correa exHumb. & Bonpl., Pyrinae.

Distinctive non-molecular features: base

chromosome number x = 17 (x = 15 inVauquelinia).

Subtribe Pyrinae Dumort. Fl. Belg.: 92

(1827): the most inclusive clade containingPyrus (as typified by Pyrus communis L.) butnot Gillenia (as typified by Gillenia trifoliata(L.) Moench), Vauquelinia (as typified by Vau-quelinia corymbosa Bonpl.), Kageneckia (astypified by Kageneckia oblonga Ruiz & Pa-v.) or Lindleya (as typified by Lindleya mes-piloides Kunth).

Included taxa: Amelanchier Medik., Aria J.Jacq., Aronia Pers., Chaenomeles Lindl., Cha-maemeles Lindl., Chamaemespilus Medik., Cor-mus Spach, Cotoneaster Medik., Crataegus L.,Cydonia Mill., Dichotomanthes Kurz, DocyniaDecne., Docyniopsis (C. K. Schneid.) Koidz.,Eriobotrya Lindl., Eriolobus Roemer, Hesperom-eles Lindl.,HeteromelesM. Roem.,MalacomelesG.N. Jones,MalusMill.,MespilusL.,OsteomelesLindl., Peraphyllum Nutt. ex Torr. & Gray,Photinia Lindl., Pseudocydonia C. K. Schneid.,Pyracantha M. Roem., Pyrus L., RhaphiolepisLindl., Sorbus L., Stranvaesia Lindl., TorminalisMedik. This subtribe corresponds to the long-recognized subfamilyMaloideae.

Distinctive non-molecular features: Hypan-

thium adnate to more than half of the ovary

(except Dichotomanthes). Stamens 20. Fruit a

pome or polypyrenous drupe. Prismatic crys-

tals in axial parenchyma. Cyanogenic glyco-sides absent in some genera (additionalsampling needed).

We gratefully acknowledge technical assis-tance from Scott Baggett, Esteban Bortiri, Fang-you Gao, and Brian Vanden Heuvel (DNAsequencing in DP’s lab), Hannah Mason andAmie Stell (fruit dissections in DRM’s lab),Wesley W. Wright (DNA sequencing in CSC’slab), and the sequencing facilities at the Univer-sity of California-Davis and the University of


Maine. Samples of Maddenia and Pygeum werekindly provided by Jun Wen. Plant material forfruit dissections was provided by Morton Arbo-retum, Arnold Arboretum, and the HarvardUniversity Herbaria. Nadia Talent provided help-ful comments on nomenclatural issues, and thediagnoses for the supertribes were translated intoLatin by Mark Garland. This work was sup-ported by NSERC grants 238505 (to RCE) andA3430 (to TAD), Swedish VR grant 621–2004–1698 (to TE), and NSF grants DEB-0089662 (toDP), DEB-0073041 (to DP and SO), and DEB-9806945 (to CSC). This is the Maine Agriculturaland Forest Experiment Station external publica-tion number 2895.

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Addresses of the authors: Daniel Potter (e-mail:[email protected]), Department of Plant Sci-ences, Mail Stop 2, University of California, OneShields Avenue, Davis, California, 95616, USA.Torsten Eriksson and Jenny E. E. Smedmark,Bergius Foundation, Royal Swedish Academy ofSciences, Box 50017, 10405 Stockholm, Sweden.Rodger C. Evans, Biology Department, AcadiaUniversity, Wolfville, Nova Scotia, Canada, B4P2R6. Sang-Hun Oh, Department of Biology, Box90338, 139 Biological Sciences, Duke University,Durham, North Carolina, 27708–0338, USA.David R. Morgan, Department of Biology, Uni-versity of West Georgia, Carrollton, Georgia,30118, USA. Malin Kerr, Department of CellBiology and Molecular Genetics, University ofMaryland, College Park, Maryland, 20742, USA.Kenneth R. Robertson, Center for Biodiversity,Illinois Natural History Survey, 1816 South OakStreet, Champaign, Illinois, 61820, USA. MathewArsenault and Christopher S. Campbell, Depart-ment of Biological Sciences, University of Maine,Orono, Maine, 04469–5735, USA. Timothy A.Dickinson, Department of Natural History, RoyalOntario Museum, 100 Queen’s Park, Toronto,Canada, M5S 2C6.


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